ARTICLE doi:10.1038/nature10922 A new hominin foot from Ethiopia shows multiple Pliocene bipedal adaptations Yohannes Haile-Selassie.2,Beverly Z.Saylor2,Alan Deino3,Naomi E.Levin4,Mulugeta Alenes Bruce M.Latimer2 A newly discovered partial hominin foot skeleton from eastern Africa indicates the presence of more than one hominin locomotor adaptation at the beginning of the Late Pliocene epoch.Here we show that new pedalelements,dated to about 3.4 million years ago,belong to a species that does not match the contemporaneous Australopithecus afarensis in its morphology and inferred locomotor adaptations,but instead are more similar to the earlier Ardipithecus ramidus in possessing an opposable great toe.This not only indicates the presence of more than one hominin species at the beginning of the Late Pliocene of eastern Africa,but also indicates the persistence of a species with Ar.ramidus-like locomotor adaptation into the Late Pliocene. Woranso-Mille is a relatively new palaeontological site located in the of other metatarsal ratios(Fig.4,see Supplementary Information for central Afar region of Ethiopia'.The fossiliferous horizons identified at discussions).Principal components analysis(PCA;correlation matrix, the site range in age from approximately 3.2 to 3.8 million years(Myr) varimax rotation with Kaiser normalization)was conducted on 11 ago.More than 54,000 fossil specimens sampling diverse mammalian metatarsal ratios(Supplementary Table 1).Although some metatarsal taxa have been collected thus far (Supplementary Information). length proportions of BRT-VP-2/73 are more similar to those of Geological and palaeontological work in the past five years has concen- cercopithecids (for example,MT2 length MT4 length)than those trated on sediments radiometrically dated to between 3.57+0.014 and 3.8+0.18 Myr ago'.These sediments have yielded numerous early hominin remains,induding a partial skeleton of Au.afarensis'-s Slightly younger deposits have subsequently yielded hominin fossils 112900 Mille R including a well-preserved,~3.4-Myr-old partial foot skeleton(BRT- VP-2/73).The detailed geological context,dating and palaeoenviron- ment ofBRT-VP-2/73 are presented in the Supplementary Information. The hominin forefoot(metatarsals and phalanges)is characteristically under-represented in the fossil record as a consequence ofits fragility in 1128 the face of predators and taphonomic processes.Previously described hominin pedal fossils-12 have not included associated and well- preserved metatarsals and phalanges.Here we describe a partial BRT-VP-2 hominin forefoot (BRT-VP-2/73)recovered from Burtele locality 2 (BRT-VP-2),one of the vertebrate localities of the Woranso-Mille 1128 study area (see Fig.1).This partial pedal skeleton is unique in provid- ing important evidence bearing on the functional morphology and proportions of several early hominin foot elements.It also presents the opportunity to draw morphological and functional comparisons between earlier (Ar.ramidus,~4.4 Myr ago)and contemporaneous 11270 (Au.afarensis,~2.9-3.6 Myr ago)hominins,and test whether there was diversity in hominin bipedalism in the earlier phases of hominin Mille-Chifra road evolutionary history3. BRT-VP-2/73 consists of eight mostly intact bony elements of a right foot:complete first,second,fourth metatarsals;head of third metatarsal;three proximal phalanges(rays 1,2 and 4);and one middle 40r3230” 4033r00r 403320” 4034700 Quatemsry sediments River ★ BRT-VP-2/73 phalanx(ray 2)(Fig.2a-fand Table 1).Detailed comparative descrip- 意Nommal fault WM07/B-1.WM10/B- tions are provided in Supplementary Information.The lack of Strike and dip 入/Messured section anatomical redundancy,spatial distribution,individual age status, morphological compatibility and preservation of the specimens indi- cate that they are from a single foot. Figure 1 Location map ofthe Burtele(BRT)vertebratelocalities(BRT-VP. 1 and BRT-VP-2)in the Woranso-Mille study area.The path ofthe measured BRT-VP-2/73 clearly differs from cercopithecids by its dorsoplantarly section through the sandstone ridges and the location of the mesa section with tall hallucal base relative to the bone's length(Fig.3a)and also relative to the dated Burtele tuff are shown.The measured basalt section is off the map the height ofthe second metatarsal base(Fig.3b),in addition to a number The study area is located about 30 miles north of Hadar and Gona. The Cleveland Museum of Natural History,Cleveland,Ohio44106,USA2Case Western Reserve University.Cleveland,Ohio 44106,USABerkeley Geochronology Center,Berkeley,California94720.USA Johns Hopkins University.Baltimore.Maryland 21218,USA.Addis Ababa University.PO Box 1176 Addis Ababa,Ethiopia. 29 MARCH 2012 VOL 483 NATURE 565 2012 Macmillan Publishers Limited.All rights reserved
ARTICLE doi:10.1038/nature10922 A new hominin foot from Ethiopia shows multiple Pliocene bipedal adaptations Yohannes Haile-Selassie1,2, Beverly Z. Saylor2 , Alan Deino3 , Naomi E. Levin4 , Mulugeta Alene5 & Bruce M. Latimer2 A newly discovered partial hominin foot skeleton from eastern Africa indicates the presence of more than one hominin locomotor adaptation at the beginning of the Late Pliocene epoch. Here we show that new pedal elements, dated to about 3.4 million years ago, belong to a species that does not match the contemporaneous Australopithecus afarensis in its morphology and inferred locomotor adaptations, but instead are more similar to the earlier Ardipithecus ramidus in possessing an opposable great toe. This not only indicates the presence of more than one hominin species at the beginning of the Late Pliocene of eastern Africa, but also indicates the persistence of a species with Ar. ramidus-like locomotor adaptation into the Late Pliocene. Woranso-Mille is a relatively new palaeontological site located in the central Afar region of Ethiopia1 . The fossiliferous horizons identified at the site range in age from approximately 3.2 to 3.8 million years (Myr) ago. More than 54,000 fossil specimens sampling diverse mammalian taxa have been collected thus far (Supplementary Information). Geological and palaeontological work in the past five years has concentrated on sediments radiometrically dated to between 3.57 6 0.014 and 3.86 0.18 Myr ago2 . These sediments have yielded numerous early hominin remains, including a partial skeleton of Au. afarensis3–5. Slightly younger deposits have subsequently yielded hominin fossils including a well-preserved, ,3.4-Myr-old partial foot skeleton (BRTVP-2/73). The detailed geological context, dating and palaeoenvironment of BRT-VP-2/73 are presented in the Supplementary Information. The homininforefoot (metatarsals and phalanges) is characteristically under-represented in the fossil record as a consequence of its fragility in the face of predators and taphonomic processes. Previously described hominin pedal fossils6–12 have not included associated and wellpreserved metatarsals and phalanges. Here we describe a partial hominin forefoot (BRT-VP-2/73) recovered from Burtele locality 2 (BRT-VP-2), one of the vertebrate localities of the Woranso-Mille study area (see Fig. 1). This partial pedal skeleton is unique in providing important evidence bearing on the functional morphology and proportions of several early hominin foot elements. It also presents the opportunity to draw morphological and functional comparisons between earlier (Ar. ramidus, ,4.4 Myr ago) and contemporaneous (Au. afarensis, ,2.9–3.6 Myr ago) hominins, and test whether there was diversity in hominin bipedalism in the earlier phases of hominin evolutionary history13. BRT-VP-2/73 consists of eight mostly intact bony elements of a right foot: complete first, second, fourth metatarsals; head of third metatarsal; three proximal phalanges (rays 1, 2 and 4); and one middle phalanx (ray 2) (Fig. 2a–f and Table 1). Detailed comparative descriptions are provided in Supplementary Information. The lack of anatomical redundancy, spatial distribution, individual age status, morphological compatibility and preservation of the specimens indicate that they are from a single foot. BRT-VP-2/73 clearly differs from cercopithecids by its dorsoplantarly tall hallucal base relative to the bone’s length (Fig. 3a) and also relative to the height of the secondmetatarsal base (Fig.3b), in addition to a number of other metatarsal ratios (Fig. 4, see Supplementary Information for discussions). Principal components analysis (PCA; correlation matrix, varimax rotation with Kaiser normalization) was conducted on 11 metatarsal ratios (Supplementary Table 1). Although some metatarsal length proportions of BRT-VP-2/73 are more similar to those of cercopithecids (for example, MT2 length , MT4 length) than those 1 The Cleveland Museum of Natural History, Cleveland, Ohio 44106, USA. 2 Case Western Reserve University, Cleveland, Ohio 44106, USA. 3 Berkeley Geochronology Center, Berkeley, California 94720, USA. 4 Johns Hopkins University, Baltimore, Maryland 21218, USA. 5 Addis Ababa University, PO Box 1176 Addis Ababa, Ethiopia. Sudan Ethiopia WORMIL Red Sea Somalia Mille R. BRT-VP-2 Waytaleyta R. Mille-Chifra road BRT-VP-1 Ridge section Offset along palaeosol Quaternary sediments Pliocene volcano sediments Pliocene basalt River Normal fault Strike and dip BRT-VP-2/73 WM07/B-1, WM10/B-1 Measured section Locality boundary 40°32′30′′ 40°33′00′′ 40°33′30′′ 40°34′00′′ 11°27′00′′ 11°27′30′′ 11°28′00′′ 11°28′30′′ 11°29′00′′ Mesa section Figure 1 | Location map of the Burtele (BRT) vertebrate localities (BRT-VP- 1 and BRT-VP-2) in theWoranso-Mille study area. The path of the measured section through the sandstone ridges and the location of the mesa section with the dated Burtele tuff are shown. The measured basalt section is off the map. The study area is located about 30 miles north of Hadar and Gona. 29 MARCH 2012 | VOL 483 | NATURE | 565 ©2012 Macmillan Publishers Limited. All rights reserved
RESEARCH ARTICLE 11118 2 cm 2 cm Figure 2 Pedal elements of BRT-VP-2/73.a,Dorsal view of all elements of hallucal proximal phalanx.e,Lateral views of the second and fourth proximal the specimen.b,Dorsal,plantar,lateral,medial,distaland proximal views of the phalanges,and the second intermediate phalanx.f,Dorsal,plantar and lateral first metatarsal.c,Dorsal,lateral,medial,proximal and distal views of the views of the fourth metatarsal.All views are from left to right. second metatarsal.d,Dorsal,lateral,plantar,distal and proximal views of the ofapes or humans,the results of the PCA clearly distinguish BRT-VP- Comparative description 2/73 from Old World monkeys and show that it falls in the cluster The hallux is represented by a complete,well-preserved,right first formed by anatomically modern humans and gorillas (Fig.4 and metatarsal (BRT-VP-2/73c)and its associated proximal phalanx Supplementary Information). (BRT-VP-2/73g;Fig.2a,b,d).The articular base of the metatarsal The proximal phalanges of BRT-VP-2/73 show the pronounced is tall,deeply concave,and it exhibits the sigmoidal configuration seen dorsal canting associated with substantial doming of its metatarsal heads in extant African apes and in Ar.ramidus".There is a low ridge similar to the condition seen in humans and early hominins such as running obliquely across the proximal articular surface from its Ar.ramidus and Au.afarensis.BRT-VP-2/73 differs from chimpanzees medial dorsoplantar midpoint to the attachment area of the fibularis by lacking long and curved metatarsal shafts(Supplementary Fig 1)and longus.A similar feature sometimes occurs in Gorilla hallucal phalanges,and in having a larger degree of dorsiflexion at the lateral metatarsals.This subdued ridge is not like that described in the metatarsophalangealjoints.It also differs from African apes by the degree proximal metatarsal base from Hadar,Ethiopia(A.L.333-54)wherein of torsion of its hallucal head(Supplementary Fig.2)and doming of its a distinct elevation nearly horizontally bisects the articular base into second and fourth metatarsal heads.BRT-VP-2/73 is similar to Ar. two semicircular facets'4.The BRT-VP-2/73c base is notably tall ramidus in showing a mosaic of derived hominin pedal characteristics relative to the bone's length,exceeding the ranges in chimpanzees associated with obligate bipedality and other features associated with and Old World monkeys,but within the ranges of gorillas and ana- arboreality.For example,it resembles Ar.ramidus in combining an tomically modern humans for this ratio(Fig.3a). abducent hallux and medially directed torsion of the second metatarsal. The BRT-VP-2/73c metatarsal head does not conform to the'typical' However,its attribution to this species would be premature particularly Australopithecus pattern in lacking the dramatic dorsal doming that in the absence of associated craniodental elements. characterizes this genus4(for example,A.L.333-115a and A.L.333-21). Table 1 Linear measurements of the pedal elements of BRT-VP-2/73 Specimen no. Element MI(mm) M2(mm) M3(mm) M4(mm) M5(mm) M6(mm) M7(mm) M8(9 BRT-VP-2/73a R.MT4 68.7 12.7 13.3 10.5 12.1 5.4 9.2 26-271 BRT-VP-2/73b R.MT2 66.9 12.8 14.2 9.8 11.2 6.05 7.35 23t BRT-VP-2/73c R.MT1 50.3 14.6 22.7 16.7 14.5 9.05 8.95 BRT-VP-2/73d R.prox.PHX 4 28.74 1025 8.6 7.9 5.4 5.32 5.16 BRT-VP-2/73e R.prox.PHX 2 29.7 10.9 9.6 7.95 5.3 6.35 6.02 BRT-VP-2/73f R.MT3 head 15.1 8.6* 13.2* BRT-VP-2/73g R.prox.PHX 1 25.23 13.1 9.73 12.24 6.5 8.45 6.06 BRT-VP-2/73h R.Int.PHX 2 18.5 926 7.63 7.3 4.4 5.1 3.85 M1.maximum length:M2proximal articular joint mediolateral:M3.proximal articular joint dorsoplantar:M4.distal articular joint mediolateral:M5.distal articular joint dorsoplantar:M6,midshatt mediolateral: M7.midshaft dorsoplantar:M8,distal head torsion. Preserved dimension. Lateral torsion in degrees Medial torsion in degrees. 566 NATURE I VOL 483 29 MARCH 2012 2012 Macmillan Publishers Limited.All rights reserved
of apes or humans, the results of the PCA clearly distinguish BRT-VP- 2/73 from Old World monkeys and show that it falls in the cluster formed by anatomically modern humans and gorillas (Fig. 4 and Supplementary Information). The proximal phalanges of BRT-VP-2/73 show the pronounced dorsal canting associated with substantial doming of its metatarsal heads similar to the condition seen in humans and early hominins such as Ar. ramidus and Au. afarensis. BRT-VP-2/73 differs from chimpanzees by lacking long and curved metatarsal shafts (Supplementary Fig. 1) and phalanges, and in having a larger degree of dorsiflexion at the lateral metatarsophalangeal joints. It also differsfromAfrican apes by the degree of torsion of its hallucal head (Supplementary Fig. 2) and doming of its second and fourth metatarsal heads. BRT-VP-2/73 is similar to Ar. ramidus in showing a mosaic of derived hominin pedal characteristics associated with obligate bipedality and other features associated with arboreality. For example, it resembles Ar. ramidus in combining an abducent hallux and medially directed torsion of the second metatarsal. However, its attribution to this species would be premature particularly in the absence of associated craniodental elements. Comparative description The hallux is represented by a complete, well-preserved, right first metatarsal (BRT-VP-2/73c) and its associated proximal phalanx (BRT-VP-2/73g; Fig. 2a, b, d). The articular base of the metatarsal is tall, deeply concave, and it exhibits the sigmoidal configuration seen in extant African apes and in Ar. ramidus11. There is a low ridge running obliquely across the proximal articular surface from its medial dorsoplantar midpoint to the attachment area of the fibularis longus. A similar feature sometimes occurs in Gorilla hallucal metatarsals. This subdued ridge is not like that described in the proximal metatarsal base from Hadar, Ethiopia (A.L. 333-54) wherein a distinct elevation nearly horizontally bisects the articular base into two semicircular facets14. The BRT-VP-2/73c base is notably tall relative to the bone’s length, exceeding the ranges in chimpanzees and Old World monkeys, but within the ranges of gorillas and anatomically modern humans for this ratio (Fig. 3a). The BRT-VP-2/73c metatarsal head does not conform to the ‘typical’ Australopithecus pattern in lacking the dramatic dorsal doming that characterizes this genus6,14 (for example,A.L. 333-115a and A.L. 333-21). a b c d e f 2 cm 2 cm 2 cm 2 cm 2 cm 2 cm Figure 2 | Pedal elements of BRT-VP-2/73. a, Dorsal view of all elements of the specimen. b, Dorsal, plantar, lateral, medial, distal and proximal views of the first metatarsal. c, Dorsal, lateral, medial, proximal and distal views of the second metatarsal. d, Dorsal, lateral, plantar, distal and proximal views of the hallucal proximal phalanx. e, Lateral views of the second and fourth proximal phalanges, and the second intermediate phalanx. f, Dorsal, plantar and lateral views of the fourth metatarsal. All views are from left to right. Table 1 | Linear measurements of the pedal elements of BRT-VP-2/73 Specimen no. Element M1 (mm) M2 (mm) M3 (mm) M4 (mm) M5 (mm) M6 (mm) M7 (mm) M8 (u) BRT-VP-2/73a R. MT4 68.7 12.7 13.3 10.5 12.1 5.4 9.2 26–27{ BRT-VP-2/73b R. MT2 66.9 12.8 14.2 9.8 11.2 6.05 7.35 23{ BRT-VP-2/73c R. MT1 50.3 14.6 22.7 16.7 14.5 9.05 8.95 – BRT-VP-2/73d R. prox. PHX 4 28.74 10.25 8.6 7.9 5.4 5.32 5.16 – BRT-VP-2/73e R. prox. PHX 2 29.7 10.9 9.6 7.95 5.3 6.35 6.02 – BRT-VP-2/73f R. MT3 head 15.1* – –8.6* 13.2* ––– BRT-VP-2/73g R. prox. PHX 1 25.23 13.1 9.73 12.24 6.5 8.45 6.06 – BRT-VP-2/73h R. Int. PHX 2 18.5 9.26 7.63 7.3 4.4 5.1 3.85 – M1, maximum length; M2, proximal articular joint mediolateral; M3, proximal articular joint dorsoplantar; M4, distal articular joint mediolateral; M5, distal articular joint dorsoplantar; M6, midshaft mediolateral; M7, midshaft dorsoplantar; M8, distal head torsion. * Preserved dimension. { Lateral torsion in degrees. { Medial torsion in degrees. RESEARCH ARTICLE 566 | NATURE | VOL 483 | 29 MARCH 2012 ©2012 Macmillan Publishers Limited. All rights reserved
ARTICLE RESEARCH b 1.00 Figure 3 Box-and-whisker plots of 0.50 1.80 0.95 pedalelement comparative ratios in 0.45 工王 cercopithecines,colobines 1.60 T 0.90 0.40 0.85 chimpanzees,gorillas,humans and 1.40 T 0.80 fossil specimens.(See 0.35 Z9S MIS S6S MIS 工 0.75 Supplementary Table 6 for 0.30 0.70 taxonomic composition.)Whisker 0.25 0.65 lines indicate maximum and 0.80 0.60 minimum values.a,Base height 0.20 (PDP)of the first metatarsal to its 0.60 0.55 0.15 0.50 length(L).b,Base height of the first nae a s metatarsal to base height of the rcopithecinae P.troglodytes Colobinae piens H. Colobinae Cercopithecinae G.gorilla P.troglodytes H.sapiens second metatarsal.c,Hallucal length to the second metatarsal length d,Hallucal length to the fourth metatarsal length.e,Base height of 1.00 e the second metatarsal to its length. 0.95 125 f,Length of the second metatarsal to 0.45 0.90 1.20 the length of the fourth metatarsal. 0.85 0.40 0.35 1.15 Measurements of the South African 0.80 and Miocene hominoids were taken 1.10 0.75 0.30 from refs 10 and 17,respectively. 1.05 0.70 0.25 0.65 0.20 T直 68 MIS 1.00 0.60 0.95 白 0.55 0.15 y 0.90 0.50 0.10 0.85 Cercopithecinae P.troglodytes Colobinae G.gorilla H.sapiens P.troglodytes Colobinae Cercopithecinae G.gorilla H.sapiens Cercopithecinae P.troglodytes Colobinae H.sapiens Its dorsoproximal articular margin is continuous and it does not hallucal segment is relatively short,falling within the ranges of exhibit the 'nonsubchondral isthmus'described in Ar.ramidus'. the African apes(Fig.3c,d)and outside the range for anatomically A simple ratio comparing the length of the first metatarsal to the modern humans(Supplementary Table 2).However,its tall hallucal lengths of the second and fourth metatarsals demonstrates that the base,relative to the shorter bases of the associated metatarsals,indi- cates that the BRT foot had a transverse arch more developed than in 3.0 apes and falls in this ratio at the higher range for anatomically modern humans (Fig.3a). ★ The hallucal proximal phalanx is essentially complete and,when 品 combined with its associated metatarsal,further confirms that the 2.5 hallucal ray is relatively short.A ratio formed between the combined ◆★ lengths of the first metatarsal and its associated proximal phalanx (MT1 PP1)and the same elements from the second ray (MT2 PP2)demonstrates that anatomically modern humans with their 2.0 elongated halluces are notably distinct.BRT-VP-2/73c falls within the ranges of apes and monkeys,indicating that the foot had a rela- 9 tively short,abductable great toe(Supplementary Fig.3).This ratio also confirms that the BRT-VP-2/73 hallucal ray was not used during 1.5 a human-like toe-off in the terminal phase of the gait cycle.However, △Cercopithecine the degree of its proximal joint canting(97)is lower than in the OColobine second ray (100),which is a condition seen in humans,whereas 公出 Gorilla the opposite is the case in chimpanzeests(Supplementary Fig.4a). 1.0 ▣Pan The second ray is represented by a metatarsal (BRT-VP-2/73b),a q4 0 大Human proximal phalanx(BRT-VP-2/73e)and an intermediate phalanx(BRT- ◆BRT-VP-2/73 VP-2/73h).BRT-VP-2/73b is a well-preserved second metatarsal.The 0 proximal base is triangular in outline.In lateral view,the base is 0.5 slightly rounded in profile (distally directed concavity)and the 0.5 1.0 1.5 2.0 2.5 3.0 3.5 shaft is longitudinally curved (Fig.2c).Relative to the bone's overall P℃1：41.2% length the dorsoplantar basal height is compressed,falling below the average for Pan,Gorilla,anatomically modern humans(Fig.3e),and Figure 4 Principal component analysis(PCA)of metatarsal ratios.Both the single reported Ar.ramidus sample (see supplementary figure 4 PCI and PC2 for 11 metatarsal ratios(descriptions of the ratios are provided in in ref.11).The dorsum of the BRT-VP-2/73 base does not exhibit Supplementary Table 1)discriminate anatomically modern humans and apes the two 'chondral invaginations'described for Ar.ramidus!. from monkeys on the one hand and chimpanzees from anatomically modern humans and gorillas on the other.BRT-VP-2/73 falls in the human/gorilla Torsion along the shaft results in the long axis of the articular head cluster.Both components are heavily influenced by ratios 6,9 and 10,which are being oriented about 23 medially from the dorsoplantar axis of the all associated exclusively with dimensions of the hallux(see Supplementary base.This torsion towards the hallux is on average less than that seen in Information for further discussion). Pan and Gorilla,but significantly more than that seen in anatomically 29 MARCH 2012 VOL 483 NATURE 567 2012 Macmillan Publishers Limited.All rights reserved
Its dorsoproximal articular margin is continuous and it does not exhibit the ‘nonsubchondral isthmus’ described in Ar. ramidus11. A simple ratio comparing the length of the first metatarsal to the lengths of the second and fourth metatarsals demonstrates that the hallucal segment is relatively short, falling within the ranges of the African apes (Fig. 3c, d) and outside the range for anatomically modern humans (Supplementary Table 2). However, its tall hallucal base, relative to the shorter bases of the associated metatarsals, indicates that the BRT foot had a transverse arch more developed than in apes and falls in this ratio at the higher range for anatomically modern humans (Fig. 3a). The hallucal proximal phalanx is essentially complete and, when combined with its associated metatarsal, further confirms that the hallucal ray is relatively short. A ratio formed between the combined lengths of the first metatarsal and its associated proximal phalanx (MT1 1 PP1) and the same elements from the second ray (MT2 1 PP2) demonstrates that anatomically modern humans with their elongated halluces are notably distinct. BRT-VP-2/73c falls within the ranges of apes and monkeys, indicating that the foot had a relatively short, abductable great toe (Supplementary Fig. 3). This ratio also confirms that the BRT-VP-2/73 hallucal ray was not used during a human-like toe-off in the terminal phase of the gait cycle. However, the degree of its proximal joint canting (97u) is lower than in the second ray (100u), which is a condition seen in humans, whereas the opposite is the case in chimpanzees15 (Supplementary Fig. 4a). The second ray is represented by a metatarsal (BRT-VP-2/73b), a proximal phalanx (BRT-VP-2/73e) and an intermediate phalanx (BRTVP-2/73h). BRT-VP-2/73b is a well-preserved second metatarsal. The proximal base is triangular in outline. In lateral view, the base is slightly rounded in profile (distally directed concavity) and the shaft is longitudinally curved (Fig. 2c). Relative to the bone’s overall length the dorsoplantar basal height is compressed, falling below the average for Pan, Gorilla, anatomically modern humans (Fig. 3e), and the single reported Ar. ramidus sample (see supplementary figure 4 in ref. 11). The dorsum of the BRT-VP-2/73 base does not exhibit the two ‘chondral invaginations’ described for Ar. ramidus11. Torsion along the shaft results in the long axis of the articular head being oriented about 23u medially from the dorsoplantar axis of the base. This torsion towards the hallux is on average less than that seen in Pan and Gorilla, but significantly more than that seen in anatomically BRT-VP-2/73 StW 562 StW 595 SKx 5017 BRT-VP-2/73 KNM-RU 2036 BRT-VP-2/73 KNM-RU 2036 BRT-VP-2/73 KNM-RU 2036 BRT-VP-2/73 StW 89 0.50 0.45 0.40 0.35 0.30 0.25 0.20 0.15 BRT-VP-2/73 Cercopithecinae Colobinae P. troglodytes G. gorilla H. sapiens MT1PDP/MT1L 1.80 1.60 1.40 1.20 1.00 0.80 0.60 Cercopithecinae Colobinae P. troglodytes G. gorilla H. sapiens MT1PDP/MT2PDP x 100 1.00 0.95 0.90 0.85 0.80 0.75 0.70 0.65 0.60 0.55 0.50 Cercopithecinae Colobinae P. troglodytes G. gorilla H. sapiens 1.00 0.95 0.90 0.85 0.80 0.75 0.70 0.65 0.60 0.55 0.50 MT1L/MT2L 0.40 0.35 0.30 0.25 0.20 0.15 0.10 0.45 1.20 1.15 1.10 1.05 1.00 0.95 0.90 0.85 MT2L/MT4L MT2PDP/MT2L MT1L/MT4L Cercopithecinae Colobinae P. troglodytes G. gorilla H. sapiens Cercopithecinae Colobinae P. troglodytes G. gorilla H. sapiens Cercopithecinae Colobinae P. troglodytes G. gorilla H. sapiens 1.25 a bc d e f Figure 3 | Box-and-whisker plots of pedal element comparative ratios in cercopithecines, colobines, chimpanzees, gorillas, humans and fossil specimens. (See Supplementary Table 6 for taxonomic composition.) Whisker lines indicate maximum and minimum values. a, Base height (PDP) of the first metatarsal to its length (L). b, Base height of the first metatarsal to base height of the second metatarsal. c, Hallucal length to the second metatarsal length. d, Hallucal length to the fourth metatarsal length. e, Base height of the second metatarsal to its length. f, Length of the second metatarsal to the length of the fourth metatarsal. Measurements of the South African and Miocene hominoids were taken from refs 10 and 17, respectively. PC 1: 41.2% 0.5 1.0 1.5 2.0 2.5 3.0 3.5 PC 2: 36.2% 3.0 2.5 2.0 1.5 1.0 0.5 BRT-VP-2/73 Human Pan Gorilla Colobine Cercopithecine Figure 4 | Principal component analysis (PCA) of metatarsal ratios. Both PC1 and PC2 for 11 metatarsal ratios (descriptions of the ratios are provided in Supplementary Table 1) discriminate anatomically modern humans and apes from monkeys on the one hand and chimpanzees from anatomically modern humans and gorillas on the other. BRT-VP-2/73 falls in the human/gorilla cluster. Both components are heavily influenced by ratios 6, 9 and 10, which are all associated exclusively with dimensions of the hallux (see Supplementary Information for further discussion). ARTICLE RESEARCH 29 MARCH 2012 | VOL 483 | NATURE | 567 ©2012 Macmillan Publishers Limited. All rights reserved
RESEARCH ARTICLE modern humans (on average this torsion ranges from neutral to 1-5 Implications for hominin pedal evolution degrees (Supplementary Fig.2)).In dorsal view (Fig.2c),the shaft Comparisons with the earlier Ar.ramidus and contemporaneous curves towards the medial side of the foot,a feature that in combination Au.afarensis provide a morphological and chronological context within with the aforementioned axial torsion acts to further direct the which to view BRT-VP-2/73.Several relevant pedal elements are also articular head towards the hallux.This complex is characteristic of represented in the South African samples from Sterkfontein and extant African apes and Ar.ramidus and is indicative of a grasping Swartkrans(see Supplementary Information for further discussion). great toe. The earlier Ar.ramidus pedal remains indicate a mosaic foot capable In contrast to the hallucal metatarsal,the superior surface morphology of terrestrial bipedal toeing-offon the lateral four metatarsophalangeal of the articular head of the second metatarsal does conform to the'typical joints (oblique metatarsal axis)while still maintaining a functionally morphological pattern shared by Ardipithecus and Australopithecus abductable,grasping hallux.By contrast,the foot of Au.afarensis In distal view,the head is roughly triangular in shape and its rounded possessed a longitudinal pedal archa permanently adducted great dorsal apex is domed above the epiphyseal junction.This dorsal toedorsal doming of its hallucal head,anteriorly canted bases doming creates the distinctive transverse gutter between the subchondral on its proximal phalanges(also shared by Ar.ramidus),and clearly margin and the diaphysis,indicating the passive hyperdorsiflexion at used a human-like transverse metatarsal axis during the latter stages of the metatarsophalangeal joint that occurs during bipedal heel-off toe-off. through toe-off6 Although BRT-VP-2/73 is contemporaneous with Au.afarensis at The articulating second proximal(BRT-VP-2/73e)and intermediate around 3.4 Myr ago(see Fig.5),it differs significantly from the known (BRT-VP-2/73h)phalanges also exhibit the derived anatomical feet of Australopithecus.Its hallux is short and the hallucal metatarsal features shared with Ar.ramidus and Au.afarensis.The base of head lacks dorsal doming.The bases of the second and fourth the proximal phalanx exhibits the dorsiflexive anterior cant (100) metatarsals of BRT-VP-2/73 do not have the expanded dorsoplantar conforming to the dorsiflexion dome of the associated metatarsal head dimensions seen in Ardipithecus and Australopithecus,features Like Ar.ramidus and Au.afarensis,the shaft exhibits strong curvature, that along with the associated rugose ligamentous attachments would although not as much as in chimpanzees(Fig.2e and Supplementary resist midtarsal and tarsometatarsal dorsiflexion and midfoot Fig.4b;see also Supplementary Information for angle measurement breaking9-23.However,its lateral metatarsophalangeal joints (MTs methods and discussions).The inclination of the proximal articular 2,3 and 4)do conform morphologically to the Ardipithecus and surface in combination with the bone's longitudinal curvature results in Australopithecus pattern,in having dorsally domed heads and an the characteristic sulcus on the dorsal surface where the articular sur- anterior cant to the phalangeal bases. facejoins the shaft.The second intermediate phalanx(BRT-VP-2/73h) BRT-VP-2/73 also resembles Ar.ramidus in combining an abducent is relatively long compared to the associated proximal phalanx(Sup- hallux and the medially directed torsion of the second metatarsal.It is plementary Table 3). also similar to Ar.ramidus and Au.afarensis in the metatarsophalangeal The third ray (BRT-VP-2/73f)is represented only by an isolated joints of the other rays,indicating that these adaptations in the lateral metatarsal head (see Fig.2a).It too conforms to the pattern seen foot are among the earliest anatomical modifications to hominin in Ardipithecus"and Australopithecus(Supplementary Fig.5)in terrestrial bipedality.The height of the hallucal metatarsal base exhibiting dorsal doming.The dorsoplantar height of the third suggests that a well-developed transverse pedal arch preceded the metatarsal head exceeds that of the second metatarsal,a relationship development of a permanent longitudinal arch.However,the lack of more common in Pan,Gorilla and Australopithecus than in anatom- dorsoplantar expansion of the metatarsal bases(MTs2 and 4)suggests ically modern humans wherein the second metatarsal head is usually that this midtarsal stabilizing feature seen in both Ar.ramidus"and taller (Supplementary Table 2). Au.afarensis was absent in this specimen. The fourth ray is represented by a complete metatarsal(BRT-VP The most surprising feature observed in the BRT-VP-2/73 forefoot 2/73g)and its associated proximal phalanx(BRT-VP 2/73d;Fig.2e,f). is the length of the fourth metatarsal relative to the first and second A ratio of the estimated dorsoplantar height of the metatarsal base and metatarsals.The currently available Ardipithecus and Australopithecus the bone's length indicates that the fourth metatarsal does not have (eastern and South African)fossil record is not adequate to assess the expanded,stabilizing base morphology seen in Au.afarensisand accurately the significance of this particular feature.However,in light Homo but,rather,is similar to Pan and some Old World monkeys of its occurrence in some Miocene apes(for example,KNM-RU 2036) (Supplementary Fig.6). it may represent the primitive state in early hominins.Nonetheless,it is The most unexpected feature seen in the fourth metatarsal is its clear that the BRT-VP-2/73 foot skeleton represents a hominin that, relative length when compared to the associated first and second unlike the contemporaneous Au.afarensis,retained a grasping capacity metatarsals.The fourth metatarsal is absolutely longer than is the that would allow it to exploit arboreal settings more effectively.Yet, second metatarsal,a condition not previously encountered in extant judging from its lateral metatarsophalangeal complex,when on the apes or hominins.The fourth metatarsal is also much longer than is ground it was at least facultatively bipedal,although it may have the hallucal metatarsal and in this ratio,the fossil specimen again fails practiced bipedality in a novel fashion probably similar to Ar.ramidus. to align with extant apes or hominins and is most similar to Old Unlike Au.afarensis,it did not have a longitudinal pedal arch,nor was World monkeys (Fig.3d,f).At present,no associated fossil elements it capable of efficiently using the transverse metatarsal axis. allow a similar comparison in Ardipithecus or Australopithecus and,as Although the taxonomic affinity of BRT-VP-2/73 is currently a consequence,no judgment can be reliably made regarding the polarity indeterminate,there is adequate morphological evidence that it does of this character.A relatively longer fourth metatarsal is the usual not belong to the contemporaneous species Au.afarensis.Regardless condition in Old World monkeys and it also occurs in some Miocene of its taxonomic affinity,however,this specimen is the first strong apes(KNM-RU 2036;ref.17),indicating that it probably represents the evidence indicating multiple hominin lineages,adaptively separated primitive condition. (at least in the foot skeleton),in the 3-4-Myr-ago time interval.A The proximal phalanx of the fourth ray(BRT-VP-2/73d;Fig.2e)is final,but important,note for the metatarsal ratios used in the PCA well preserved and similar to those observed in Ardipithecus"and performed in this study,anatomically modern humans and gorillas Australopithecus.It has the shallow transverse sulcus where the overlap substantially and BRT-VP-2/73 falls in the gorilla cluster.It proximal articular surface cants anteriorly into the curvature of the is unclear at this point what the functional implications of this overlap shaft.It presents a higher degree of dorsal canting than does the might mean;it requires further investigation as it has important con- phalanx of the second ray (104,see Supplementary Fig.4a and sequences for the interpretation of locomotor behaviour in early Supplementary Information for discussions). hominins. 568 NATUREI VOL 483 29 MARCH 2012 2012 Macmillan Publishers Limited.All rights reserved
modern humans (on average this torsion ranges from neutral to 1–5 degrees (Supplementary Fig. 2)). In dorsal view (Fig. 2c), the shaft curves towards the medial side of the foot, a feature that in combination with the aforementioned axial torsion acts to further direct the articular head towards the hallux. This complex is characteristic of extant African apes and Ar. ramidus and is indicative of a grasping great toe. In contrast to the hallucal metatarsal, the superior surface morphology of the articular head of the secondmetatarsal does conform to the ‘typical’ morphological pattern shared byArdipithecus and Australopithecus6,12,16. In distal view, the head is roughly triangular in shape and its rounded dorsal apex is domed above the epiphyseal junction. This dorsal doming creates the distinctive transverse gutter between the subchondral margin and the diaphysis, indicating the passive hyperdorsiflexion at the metatarsophalangeal joint that occurs during bipedal heel-off through toe-off11,16. The articulating second proximal (BRT-VP-2/73e) and intermediate (BRT-VP-2/73h) phalanges also exhibit the derived anatomical features shared with Ar. ramidus11 and Au. afarensis6,12. The base of the proximal phalanx exhibits the dorsiflexive anterior cant (100u) conforming to the dorsiflexion dome of the associated metatarsal head. Like Ar. ramidus and Au. afarensis, the shaft exhibits strong curvature, although not as much as in chimpanzees (Fig. 2e and Supplementary Fig. 4b; see also Supplementary Information for angle measurement methods and discussions). The inclination of the proximal articular surface in combination with the bone’s longitudinal curvature results in the characteristic sulcus on the dorsal surface where the articular surface joins the shaft. The second intermediate phalanx (BRT-VP-2/73h) is relatively long compared to the associated proximal phalanx (Supplementary Table 3). The third ray (BRT-VP-2/73f) is represented only by an isolated metatarsal head (see Fig. 2a). It too conforms to the pattern seen in Ardipithecus11 and Australopithecus6 (Supplementary Fig. 5) in exhibiting dorsal doming. The dorsoplantar height of the third metatarsal head exceeds that of the second metatarsal, a relationship more common in Pan, Gorilla and Australopithecus than in anatomically modern humans wherein the second metatarsal head is usually taller (Supplementary Table 2). The fourth ray is represented by a complete metatarsal (BRT-VP 2/73g) and its associated proximal phalanx (BRT-VP 2/73d; Fig. 2e, f). A ratio of the estimated dorsoplantar height of the metatarsal base and the bone’s length indicates that the fourth metatarsal does not have the expanded, stabilizing base morphology seen in Au. afarensis12 and Homo but, rather, is similar to Pan and some Old World monkeys (Supplementary Fig. 6). The most unexpected feature seen in the fourth metatarsal is its relative length when compared to the associated first and second metatarsals. The fourth metatarsal is absolutely longer than is the second metatarsal, a condition not previously encountered in extant apes or hominins. The fourth metatarsal is also much longer than is the hallucal metatarsal and in this ratio, the fossil specimen again fails to align with extant apes or hominins and is most similar to Old World monkeys (Fig. 3d, f). At present, no associated fossil elements allow a similar comparison inArdipithecus orAustralopithecus and, as a consequence, no judgment can be reliably made regarding the polarity of this character. A relatively longer fourth metatarsal is the usual condition in Old World monkeys and it also occurs in some Miocene apes (KNM-RU 2036; ref. 17), indicating that it probably represents the primitive condition. The proximal phalanx of the fourth ray (BRT-VP-2/73d; Fig. 2e) is well preserved and similar to those observed in Ardipithecus11 and Australopithecus6,16. It has the shallow transverse sulcus where the proximal articular surface cants anteriorly into the curvature of the shaft. It presents a higher degree of dorsal canting than does the phalanx of the second ray (104u, see Supplementary Fig. 4a and Supplementary Information for discussions). Implications for hominin pedal evolution Comparisons with the earlier Ar. ramidus and contemporaneous Au. afarensis provide a morphological and chronological context within which to view BRT-VP-2/73. Several relevant pedal elements are also represented in the South African samples from Sterkfontein and Swartkrans10 (see Supplementary Information for further discussion). The earlierAr. ramidus pedal remains indicate a mosaicfoot capable of terrestrial bipedal toeing-off on the lateral four metatarsophalangeal joints (oblique metatarsal axis11) while still maintaining a functionally abductable, grasping hallux. By contrast, the foot of Au. afarensis possessed a longitudinal pedal arch6,12,18, a permanently adducted great toe12,14,16, dorsal doming of its hallucal head6,14, anteriorly canted bases on its proximal phalanges6,16 (also shared byAr. ramidus11), and clearly used a human-like transverse metatarsal axis during the latter stages of toe-off. Although BRT-VP-2/73 is contemporaneous with Au. afarensis at around 3.4 Myr ago (see Fig. 5), it differs significantly from the known feet of Australopithecus. Its hallux is short and the hallucal metatarsal head lacks dorsal doming. The bases of the second and fourth metatarsals of BRT-VP-2/73 do not have the expanded dorsoplantar dimensions seen in Ardipithecus11 and Australopithecus12,14, features that along with the associated rugose ligamentous attachments would resist midtarsal and tarsometatarsal dorsiflexion and midfoot breaking19–23. However, its lateral metatarsophalangeal joints (MTs 2, 3 and 4) do conform morphologically to the Ardipithecus and Australopithecus pattern, in having dorsally domed heads and an anterior cant to the phalangeal bases. BRT-VP-2/73 also resembles Ar. ramidus in combining an abducent hallux and the medially directed torsion of the second metatarsal. It is also similar toAr. ramidus andAu. afarensisin the metatarsophalangeal joints of the other rays, indicating that these adaptations in the lateral foot are among the earliest anatomical modifications to hominin terrestrial bipedality. The height of the hallucal metatarsal base suggests that a well-developed transverse pedal arch preceded the development of a permanent longitudinal arch. However, the lack of dorsoplantar expansion of the metatarsal bases (MTs 2 and 4) suggests that this midtarsal stabilizing feature seen in both Ar. ramidus11 and Au. afarensis12 was absent in this specimen. The most surprising feature observed in the BRT-VP-2/73 forefoot is the length of the fourth metatarsal relative to the first and second metatarsals. The currently available Ardipithecus and Australopithecus (eastern and South African) fossil record is not adequate to assess accurately the significance of this particular feature. However, in light of its occurrence in some Miocene apes (for example, KNM-RU 2036) it may represent the primitive state in early hominins. Nonetheless, it is clear that the BRT-VP-2/73 foot skeleton represents a hominin that, unlike the contemporaneous Au. afarensis, retained a grasping capacity that would allow it to exploit arboreal settings more effectively. Yet, judging from its lateral metatarsophalangeal complex, when on the ground it was at least facultatively bipedal, although it may have practiced bipedality in a novel fashion probably similar to Ar. ramidus. Unlike Au. afarensis, it did not have a longitudinal pedal arch, nor was it capable of efficiently using the transverse metatarsal axis. Although the taxonomic affinity of BRT-VP-2/73 is currently indeterminate, there is adequate morphological evidence that it does not belong to the contemporaneous species Au. afarensis. Regardless of its taxonomic affinity, however, this specimen is the first strong evidence indicating multiple hominin lineages, adaptively separated (at least in the foot skeleton), in the 3–4-Myr-ago time interval. A final, but important, note for the metatarsal ratios used in the PCA performed in this study, anatomically modern humans and gorillas overlap substantially and BRT-VP-2/73 falls in the gorilla cluster. It is unclear at this point what the functional implications of this overlap might mean; it requires further investigation as it has important consequences for the interpretation of locomotor behaviour in early hominins. RESEARCH ARTICLE 568 | NATURE | VOL 483 | 29 MARCH 2012 ©2012 Macmillan Publishers Limited. All rights reserved
ARTICLE RESEARCH Burtele(BRT) 2.Deino,A.Letal.40Ar/39Ar dating paleomagnetism,and tephrochemistry of Soil Pliocene strata of the hominid-bearing Woranso-Mille area,west-central Afar Rift. 30 Ethiopia.J.Hum.Evol.58,111-126(2010). .n ..Pebbly sandstone Haile-Selassie,Y.,Saylor,B.Z,Deino,A.,Alene,M.&Latimer,B.New hominid fossils a Coarse sandstone from Woranso-Mille(Central Afar,Ethiopia)the taxonomy ofearly Australopithecus. Am.J.Phys.Anthropol.141,406-417(2009). 4 ▣ Flaggy sandstone 4. Haile-Selassie,Y.et al.An early Australopithecus afarensis postcranium from Woranso-Mille,Ethiopia.Proc.Nat/Acad.Sci.USA 107,12121-12126(2010) 5. Haile-Selassie,Y.Phylogeny of early Australopithecus:new fossil evidence from the WM11-BRT-141 口 Mudstone and sandstone Woranso-Mille (Central Afar,Ethiopia).Phil Trans.R.Soc.B 365,3323-3331 bbb Basalt (2010). 6. Latimer,B.M.Lovejoy,C.O.Hominid tarsal,metatarsal,and phalangeal bones 20 ⊙ Gastropod layer recovered from the e Ha ar formation:1974-1977 collections.Am.J.Phys. Anthropol.57,701-719(1982). Planar laminations 1 Day,M.H.Napier,J.R.Hominid fossils from Bed l,Olduvai Gorge,Tanganyika: PL. Parting lineations fossil footbones.Nature 201,969-970 (1964). 三P Zipfel,B.et al.The foot and ankle of Australopithecus sediba.Science 333, Ripple stratification 1417-1420(2011) WM11-BRT-140 9. Clarke.R.J.Tobias.P.V.Sterkfontein Member 2 foot bones of the oldest South w Trough-cross bedding African hominid.Science 269,521-524 (1995) 10.Deloison,Y.Anatomie des os fossiles de pieds des hominides d'Afrique du Sud. 0 Soil carbonate sample Biomet Hum.Anthropol.21,189-230(2003) Altered tuff 11.Lovejoy.O.C.,Latimer,B.Suwa,G.Asfaw,B.White,T.D.Combining prehension and propulsion:The foot of Ardipithecus ramidus.Science 326,72(2009) ★ BRT-VP-2/73 12.Ward,C.V Kimbel,W.H.Johanson,D.C.Complete fourth metatarsal and arches in the foot of Australooithecus afarensis.Science 331,750-753(2011). Vertebrate fossil 13.Harcourt-Smith,W.E.H.Aiello,L C.Fossils,feet and the evolution of human horizon bipedal locomotion.J.Anat 204.403-416 (2004). 画N⑨ 14. Latimer,B.M.Lovejoy,C.O.Hallucal tarsometatarsal joint in Australopithecus Burtele tuff:3.469+0.008 Myr ago afarensis.Am.J.Phys.Anthropol.82,125-133(1990). (average of WM07/B-1 and WM10/B-1) 15.Griffin,N.L&Richmond,B.G.Joint orientation and function in great ape and human proximal pedal phalanges.Am.J.Phys.Anthropol.141,116-123(2010) 16.Latimer,B.M.&Lovejoy.C.O.Metatarsophalangeal joints of Australopithecus bbbb afarensis.Am.J.Phys.Anthropol.83,13-23(1990). 17.Walker,A C.Pickford,M.in New Interpretaions of Ape and Human Ancestry (eds Ciochon,R.L.Corruccini.R.S.)325-413(Plenum,1983) 18.White,T.D.Suwa.G.Hominid footprints at Laetoli:facts and interpretations.Am. Figure 5Stratigraphic section at the BRT localities and placement of the Phys.Anthropol.72,485-514(1987). 19.Elftman,H.Manter.J.Chimpanzee and human feet in bipedal walking.Am.J. BRT-VP-2/73 partial foot skeleton.The Burtele tuff is dated by the Ar/Ar Phys.Anthropol 20,69-79(1935). method to 3.469+0.008 Myr ago and lies a maximum of about 27 m below 20.Elftman,H.Manter,J.The evolution of the human foot with special reference to BRT-VP-2/73,providing a maximum age constraint of ~3.47 Myr ago for the the joints.J.Anat.70,56-67 (1935). foot specimen (shown by the black star)and for three fossiliferous sandstone 21 DeSilva,J.M.Functional morphology of the ankle and the likelihood of climbing in horizons (shown by vertical lines)at BRT-VP-1 and BRT-VP-2.An 22. approximate age for the foot specimen,using regional sediment accumulation DeeVaSegment and joint angles of hind limb during bipedal and quadrupedal walking of the bonobo rates,suggests an age of between 3.2 and 3.4 Myr ago for BRT-VP-2/73(see (Pan paniscus).Am.J.Phys.Anthropol.119,37-51(2002). Methods for details).S,F,M,C,P indicates soil,flaggy,mudstone,coarse and 23.Vereecke,E D'Aout,K..De Clercg.D..Van Elsacker,L&Aerts,P.Dynamic plantar pebbly sandstone,respectively;it shows the degree of resistance to erosion and pressure distribution during terrestrial locomotion of bonobos(Pan paniscus).Am. rock stiffness. J.Phys.Anthropol.120,373-383(2003). 24.Walter,R.C.Aronson,J.L.Age and source of the Sidi Hakoma Tuff,Hadar METHODS SUMMARY Formation,Ethiopia.J.Hum.Evol.25,229-240(1993). 25.deMenocal,P.B.Brown,F.H.in Hominid Evolution and Climatic Change in Europe The Burtele tuff at the base of the section is dated by the 4Ar/Ar method to (eds Agusti,J.Rook,L Andrews,P.)23-54(Cambridge Univ.Press,1999). 3.4690.008 Myr ago (analytical data are given in Supplementary Information) 26.McDougall,I.Brown,F.H.Geochronology of the pre-KBS Tuff sequence,Omo and lies a maximum ofabout 27 m below BRT-VP-2/73,providing a firm maximum Group,Turkana Basin.J.Geol.Soc Lond165,549-562(2008) age constraint of~3.47 Myr ago for the foot specimen(Fig.5).An approximate age 27.Passey,B.H.,Levin,N.E.Cerling.T.E Brown,F.H.Eiler,J.M.High-temperature environments of human evolution in East Africa based on bond ordering in for the foot specimen can be estimated using regional sediment accumulation rates paleosol carbonates.Proc.Natl Acad.Sci.USA 107,11245-11249 (2010). The average rate for older WORMIL strata in the Waki-Mille confluence area is 11 cm kyr(ref.2),which yields an estimated age of 3.22 Myr ago for the BRT-VP- Supplementary Information is linked to the online version of the paper at 2/73 specimen.This rate is much lower than estimates for the Sidi Hakoma Member www.nature.com/nature. of the Hadar Formation,which is closer in age to the BRT ridge section,but is Acknowledgements We thank the Authority for Research and Conservation of Cultural much farther away geographically.Using a Sidi Hakoma accumulation rate of Heritage and the Afar Regional State of Ethiopia for permission to conduct field and 30 cm kyr yields an estimate of3.38 Myr ago for BRT-VP-2/73.These contrasting laboratory research,and the Afar people of the Woranso-Mille area for support in the rates indicate an age of between 3.2 and 3.4 Myr ago for BRT-VP-2/73. field.We also thank M.Asnake,R.Bernor.S.Frost,D.Geraads,I.Giaourtsakis,M.Lewis. W.Sanders and L Werdelin for faunal identifications We thank B.Passey for aid with For the isotopic analysis of pedogenic carbonate,carbonate nodules were isotope analyses;E.Guthrie for unpublished primary data;L Russell for photography; sampled from peds with slickenside surfaces and clay cutans,within a distinct S.Melillo and H.Gebreyesus for fieldwork:O.Lovejoy,S.Simpson,G.Suwa andT.White pedogenic carbonate zone,250 cm below the palaeosol contact with the over- for comments and discussions;D.Su for discussions and assistance in statistical lying silt.C,O and A measurements of carbonate were made using an analysis;and L Jellema for assistance in photography.This research was supported by automated common acid bath peripheral coupled to a Thermo MAT 253 mass funding from the LSB Leakey Foundation,the National Geographic Society.the Cleveland Museum of Natural History,and NSF grants BCS-0234320,BCS-0321893 spectrometer at Johns Hopkins University,using methods described previously27 BCS-0542037 and BCS-1124705. The results are reported in Supplementary Table 8. Author Contributions Y.H.-S.and B.M.L conducted the description and comparative Full Methods and any associated references are available in the online version of analysis.B.Z.S.,N.E.L and M.A compiled the stratigraphic sequence.A.D.conducted the paper at www.nature.com/nature. the radiometric dating.N.E.L conducted stable isotope analysis.Y.H.-S.and B.M.L wrote the paper with input from all authors. Received 22 October 2011;accepted 8 February 2012. Author Information Reprints and permissions information is available at www.nature.com/reprints.The authors declare no competing financial interests. 1.Haile-Selassie,Y.Deino,A,Saylor,B..Umer,M.Latimer,B.Preliminary geology Readers are welcome to comment on the online version of this arcle at and paleontology of new hominid-bear g Pliocene localities in the central Afar www.nature.com/nature.Correspondence and requests for materials should be region of Ethiopia.Anthropol Sci.115,215-222 (2007). addressed to Y.H.-S.(yhailese@cmnh.org). 29 MARCH 2012 VOL 483 NATURE 569 2012 Macmillan Publishers Limited.All rights reserved
METHODS SUMMARY The Burtele tuff at the base of the section is dated by the 40Ar/39Ar method to 3.4696 0.008 Myr ago (analytical data are given in Supplementary Information) and lies a maximum of about 27 m below BRT-VP-2/73, providing afirmmaximum age constraint of ,3.47Myr ago for the foot specimen (Fig. 5). An approximate age for the foot specimen can be estimated using regional sediment accumulation rates. The average rate for older WORMIL strata in the Waki-Mille confluence area is 11 cm kyr21 (ref. 2), which yields an estimated age of 3.22 Myr ago for the BRT-VP- 2/73 specimen. This rate is much lower than estimatesfor the Sidi Hakoma Member of the Hadar Formation24–26, which is closer in age to the BRT ridge section, but is much farther away geographically. Using a Sidi Hakoma accumulation rate of 30 cm kyr21 yields an estimate of 3.38Myr ago for BRT-VP-2/73. These contrasting rates indicate an age of between 3.2 and 3.4 Myr ago for BRT-VP-2/73. For the isotopic analysis of pedogenic carbonate, carbonate nodules were sampled from peds with slickenside surfaces and clay cutans, within a distinct pedogenic carbonate zone, $50 cm below the palaeosol contact with the overlying silt. d13C, d18O and D47 measurements of carbonate were made using an automated common acid bath peripheral coupled to a Thermo MAT 253 mass spectrometer at Johns Hopkins University, using methods described previously27. The results are reported in Supplementary Table 8. Full Methods and any associated references are available in the online version of the paper at www.nature.com/nature. Received 22 October 2011; accepted 8 February 2012. 1. Haile-Selassie, Y., Deino, A., Saylor, B., Umer, M. & Latimer, B. Preliminary geology and paleontology of new hominid-bearing Pliocene localities in the central Afar region of Ethiopia. Anthropol. Sci. 115, 215–222 (2007). 2. Deino, A. L. et al. 40Ar/39Ar dating, paleomagnetism, and tephrochemistry of Pliocene strata of the hominid-bearing Woranso-Mille area, west-central Afar Rift, Ethiopia. J. Hum. Evol. 58, 111–126 (2010). 3. Haile-Selassie, Y., Saylor,B. Z., Deino, A., Alene,M. & Latimer, B. New hominid fossils fromWoranso-Mille (Central Afar, Ethiopia) the taxonomy of earlyAustralopithecus. Am. J. Phys. Anthropol. 141, 406–417 (2009). 4. Haile-Selassie, Y. et al. An early Australopithecus afarensis postcranium from Woranso-Mille, Ethiopia. Proc. Natl Acad. Sci. USA 107, 12121–12126 (2010). 5. Haile-Selassie, Y. Phylogeny of early Australopithecus: new fossil evidence from the Woranso-Mille (Central Afar, Ethiopia). Phil. Trans. R. Soc. B 365, 3323–3331 (2010). 6. Latimer, B. M. & Lovejoy, C. O. Hominid tarsal, metatarsal, and phalangeal bones recovered from the Hadar formation: 1974–1977 collections. Am. J. Phys. Anthropol. 57, 701–719 (1982). 7. Day, M. H. & Napier, J. R. Hominid fossils from Bed I, Olduvai Gorge, Tanganyika: fossil footbones. Nature 201, 969–970 (1964). 8. Zipfel, B. et al. The foot and ankle of Australopithecus sediba. Science 333, 1417–1420 (2011). 9. Clarke, R. J. & Tobias, P. V. Sterkfontein Member 2 foot bones of the oldest South African hominid. Science 269, 521–524 (1995). 10. Deloison, Y. Anatomie des os fossiles de pieds des hominides d’Afrique du Sud. Biomet. Hum. Anthropol. 21, 189–230 (2003). 11. Lovejoy, O. C., Latimer, B., Suwa, G., Asfaw, B. & White, T. D. Combining prehension and propulsion: The foot of Ardipithecus ramidus. Science 326, 72 (2009). 12. Ward, C. V., Kimbel, W. H. & Johanson, D. C. Complete fourthmetatarsal and arches in the foot of Australopithecus afarensis. Science 331, 750–753 (2011). 13. Harcourt-Smith, W. E. H. & Aiello, L. C. Fossils, feet and the evolution of human bipedal locomotion. J. Anat. 204, 403–416 (2004). 14. Latimer, B. M. & Lovejoy, C. O. Hallucal tarsometatarsal joint in Australopithecus afarensis. Am. J. Phys. Anthropol. 82, 125–133 (1990). 15. Griffin, N. L. & Richmond, B. G. Joint orientation and function in great ape and human proximal pedal phalanges. Am. J. Phys. Anthropol. 141, 116–123 (2010). 16. Latimer, B. M. & Lovejoy, C. O. Metatarsophalangeal joints of Australopithecus afarensis. Am. J. Phys. Anthropol. 83, 13–23 (1990). 17. Walker, A. C. & Pickford, M. in New Interpretaions of Ape and Human Ancestry (eds Ciochon, R. L. & Corruccini, R. S.) 325–413 (Plenum, 1983). 18. White, T. D. & Suwa, G. Hominid footprints at Laetoli: facts and interpretations. Am. J. Phys. Anthropol. 72, 485–514 (1987). 19. Elftman, H. & Manter, J. Chimpanzee and human feet in bipedal walking. Am. J. Phys. Anthropol. 20, 69–79 (1935). 20. Elftman, H. & Manter, J. The evolution of the human foot with special reference to the joints. J. Anat. 70, 56–67 (1935). 21. DeSilva, J. M. Functional morphology of the ankle and the likelihood of climbing in early hominins. Proc. Natl Acad. Sci. USA 106, 6567–6572 (2009). 22. D’Aout, K., Aerts, P., De Clercq, D., De Meester, K. & Van Elsacker, L. Segment and joint angles of hind limb during bipedal and quadrupedal walking of the bonobo (Pan paniscus). Am. J. Phys. Anthropol. 119, 37–51 (2002). 23. Vereecke, E., D’Aout, K., De Clercq, D., Van Elsacker, L. & Aerts, P. Dynamic plantar pressure distribution during terrestrial locomotion of bonobos (Pan paniscus). Am. J. Phys. Anthropol. 120, 373–383 (2003). 24. Walter, R. C. & Aronson, J. L. Age and source of the Sidi Hakoma Tuff, Hadar Formation, Ethiopia. J. Hum. Evol. 25, 229–240 (1993). 25. deMenocal, P. B. & Brown, F. H. in Hominid Evolution and Climatic Change in Europe (eds Agusti, J., Rook, L. & Andrews, P.) 23–54 (Cambridge Univ. Press, 1999). 26. McDougall, I. & Brown, F. H. Geochronology of the pre-KBS Tuff sequence, Omo Group, Turkana Basin. J. Geol. Soc. Lond. 165, 549–562 (2008). 27. Passey, B. H., Levin, N. E., Cerling, T. E., Brown, F. H. & Eiler, J. M. High-temperature environments of human evolution in East Africa based on bond ordering in paleosol carbonates. Proc. Natl Acad. Sci. USA 107, 11245–11249 (2010). Supplementary Information is linked to the online version of the paper at www.nature.com/nature. Acknowledgements We thank the Authority for Research and Conservation of Cultural Heritage and the Afar Regional State of Ethiopia for permission to conduct field and laboratory research, and the Afar people of the Woranso-Mille area for support in the field. We also thank M. Asnake, R. Bernor, S. Frost, D. Geraads, I. Giaourtsakis, M. Lewis, W. Sanders and L. Werdelin for faunal identifications. We thank B. Passey for aid with isotope analyses; E. Guthrie for unpublished primary data; L. Russell for photography; S. Melillo and H. Gebreyesus for fieldwork; O. Lovejoy, S. Simpson, G. Suwa and T. White for comments and discussions; D. Su for discussions and assistance in statistical analysis; and L. Jellema for assistance in photography. This research was supported by funding from the LSB Leakey Foundation, the National Geographic Society, the Cleveland Museum of Natural History, and NSF grants BCS-0234320, BCS-0321893, BCS-0542037 and BCS-1124705. Author Contributions Y.H.-S. and B.M.L. conducted the description and comparative analysis. B.Z.S., N.E.L. and M.A. compiled the stratigraphic sequence. A.D. conducted the radiometric dating. N.E.L. conducted stable isotope analysis. Y.H.-S. and B.M.L. wrote the paper with input from all authors. Author Information Reprints and permissions information is available at www.nature.com/reprints. The authors declare no competing financial interests. Readers are welcome to comment on the online version of this article at www.nature.com/nature. Correspondence and requests for materials should be addressed to Y.H.-S. (yhailese@cmnh.org). Soil Pebbly sandstone Coarse sandstone Flaggy sandstone Mudstone and sandstone Basalt Gastropod layer Planar laminations Parting lineations Ripple stratification Trough-cross bedding Soil carbonate sample Altered tuff Vertebrate fossil horizon BRT-VP-2/73 Burtele tuff: 3.469 ± 0.008 Myr ago (average of WM07/B-1 and WM10/B-1) S F MCP Mesa 0 m 10 20 30 Sandstone ridges of BRT-VP-1,2 Burtele (BRT) WM11-BRT-141 WM11-BRT-140 P.L. P.L. Figure 5 | Stratigraphic section at the BRT localities and placement of the BRT-VP-2/73 partial foot skeleton. The Burtele tuff is dated by the 40Ar/39Ar method to 3.469 6 0.008 Myr ago and lies a maximum of about 27 m below BRT-VP-2/73, providing a maximum age constraint of ,3.47 Myr ago for the foot specimen (shown by the black star) and for three fossiliferous sandstone horizons (shown by vertical lines) at BRT-VP-1 and BRT-VP-2. An approximate age for the foot specimen, using regional sediment accumulation rates, suggests an age of between 3.2 and 3.4Myr ago for BRT-VP-2/73 (see Methods for details). S, F, M, C, P indicates soil, flaggy, mudstone, coarse and pebbly sandstone, respectively; it shows the degree of resistance to erosion and rock stiffness. ARTICLE RESEARCH 29 MARCH 2012 | VOL 483 | NATURE | 569 ©2012 Macmillan Publishers Limited. All rights reserved
RESEARCH ARTICLE METHODS Burtele tuff.The plagioclase weighted-mean age of sample WM10/B-1 is 40Ar/39Ar dating procedures follow those of ref.2.The mineral separates were predictably less precise than either K-feldspar age,due to the lower potassium irradiated for 5h in two separate batches in the in-core CLICIT facility of the content,but is nevertheless a reasonable result (3.420.03 Myr)that is not Oregon State University TRIGA reactor.Sanidine from the Fish Canyon Tuff of statistically different from the K-feldspar age. Colorado was used as a monitor mineral,with an age of 28.201 Myr2.After irra- The Burtele tuff at the base of the section is dated by the4Ar/Ar method to diation,the feldspar grains were individually analysed under ultra-high vacuum on 3.469+0.008 Myr ago (analytical data are given in Supplementary Information) a MAP 215 Noble-gas mass spectrometer,using a focused CO2 laser as the heating and lies a maximum of about 27m below BRT-VP-2/73,providing a firm device.In all,56 grains were analysed from the two samples(Supplementary Table maximum age constraint of~3.47 Myr ago for the foot specimen.An approximate 7).Most grains(34)provedtobe K-feldspar,asjudgedby theCa/K ratiodetermined age for the foot specimen can be estimated using regional sediment accumulation from the measured argon isotopes,whereas the remainder were relatively low-Ca/K rates.The average rate for older WORMIL strata in the Waki-Mille confluence area plagioclase.Most analyses yielded the anticipated high proportion of radiogenic is 11 cmkyr(ref.2),which yields an estimated age of 3.22 Myr ago for the BRT- r relative to atmosphericAr contamination expected for unaltered feldspars VP-2/73 specimen.This rate is much lower than estimates for the Sidi Hakoma from Pliocene volcanic rocks,but a few exhibited anomalously low radiogenic Member of the Hadar Formation2-,which is closer in age to the BRT ridge content,and were excluded from further analysis;an arbitrary cutoff of 60% section,but is much farther away geographically.Using a Sidi Hakoma accumula- Arwas used,identifying four grains for exclusion.In addition,as is typical for tion rate of 30 cmkyr yields an estimate of 3.38 Myr for BRT-VP-2/73.These East African tephra,a slight tail of the age distribution towards older ages was contrasting rates suggest an age of between 3.2 and 3.4 Myr ago for BRT-VP-2/73. observed.A statistical filter was applied to the sample distributions,using a median For the isotopic analysis of pedogenic carbonate,carbonate nodules were outlier determinant(outliers were classified as falling 1.5 normalized median abso- sampled from peds with slickenside surfaces and clay cutans,within a distinct lute deviations'from the median).Use of this criterion identified three outliers in pedogenic carbonate zone,250 cm below the palaeosol contact with the over- each of WM07/B-1 (K-feldspar)and WM10/B-1 (Plagioclase).The remaining lying silt.C.O and A measurements of carbonate were made using an populations yield simple,unimodal Gaussian-like distributions(Supplementary automated common acid bath peripheral coupled to a Thermo MAT 253 mass Fig.7).Weighted-mean sample ages of the K-feldspar populations from samples spectrometer at Johns Hopkins University,using methods described previously2? WM07/B-1 and WM10/B-I are 3.4840.011 Myr(n 24;1o analytical error, The results are reported in Supplementary Table 8. incorporating error in /the neutron fluence parameter of0.2%)and 3.453+0.011 Myr (n=4),respectively (Supplementary Table 4).An overall weighted-mean of 28.Kuiper,K.F.et al Synchronizing rock clocks of earth history.Science 320, the two K-feldspar ages is 3.469+0.008 Myr,taken as the reference age for the 500-504(2008). 2012 Macmillan Publishers Limited.All rights reserved
METHODS 40Ar/39Ar dating procedures follow those of ref. 2. The mineral separates were irradiated for 5 h in two separate batches in the in-core CLICIT facility of the Oregon State University TRIGA reactor. Sanidine from the Fish Canyon Tuff of Colorado was used as a monitor mineral, with an age of 28.201Myr28. After irradiation, the feldspar grains were individually analysed under ultra-high vacuum on a MAP 215 Noble-gas mass spectrometer, using a focused CO2 laser as the heating device. In all, 56 grains were analysed from the two samples (Supplementary Table 7).Most grains (34) proved to be K-feldspar, as judged by the Ca/K ratio determined from the measured argon isotopes, whereas the remainder were relatively low-Ca/K plagioclase. Most analyses yielded the anticipated high proportion of radiogenic 40Ar relative to atmospheric 40Ar contamination expected for unaltered feldspars from Pliocene volcanic rocks, but a few exhibited anomalously low radiogenic content, and were excluded from further analysis; an arbitrary cutoff of 60% 40Ar* was used, identifying four grains for exclusion. In addition, as is typical for East African tephra, a slight tail of the age distribution towards older ages was observed. A statistical filter was applied to the sample distributions, using a median outlier determinant (outliers were classified as falling 1.5 ‘normalized median absolute deviations’ from the median). Use of this criterion identified three outliers in each of WM07/B-1 (K-feldspar) and WM10/B-1 (Plagioclase). The remaining populations yield simple, unimodal Gaussian-like distributions (Supplementary Fig. 7). Weighted-mean sample ages of the K-feldspar populations from samples WM07/B-1 and WM10/B-1 are 3.484 6 0.011 Myr (n 5 24; 1s analytical error, incorporating error in J, the neutron fluence parameter of 0.2%) and 3.453 6 0.011 Myr (n 5 4), respectively (Supplementary Table 4). An overall weighted-mean of the two K-feldspar ages is 3.469 6 0.008Myr, taken as the reference age for the Burtele tuff. The plagioclase weighted-mean age of sample WM10/B-1 is predictably less precise than either K-feldspar age, due to the lower potassium content, but is nevertheless a reasonable result (3.42 6 0.03 Myr) that is not statistically different from the K-feldspar age. The Burtele tuff at the base of the section is dated by the 40Ar/39Ar method to 3.469 6 0.008 Myr ago (analytical data are given in Supplementary Information) and lies a maximum of about 27 m below BRT-VP-2/73, providing a firm maximum age constraint of ,3.47Myr ago for the foot specimen. An approximate age for the foot specimen can be estimated using regional sediment accumulation rates. The average rate for olderWORMIL strata in the Waki-Mille confluence area is 11 cm kyr21 (ref. 2), which yields an estimated age of 3.22Myr ago for the BRTVP-2/73 specimen. This rate is much lower than estimates for the Sidi Hakoma Member of the Hadar Formation24–26, which is closer in age to the BRT ridge section, but is much farther away geographically. Using a Sidi Hakoma accumulation rate of 30 cm kyr21 yields an estimate of 3.38Myr for BRT-VP-2/73. These contrasting rates suggest an age of between 3.2 and 3.4 Myr ago for BRT-VP-2/73. For the isotopic analysis of pedogenic carbonate, carbonate nodules were sampled from peds with slickenside surfaces and clay cutans, within a distinct pedogenic carbonate zone, $50 cm below the palaeosol contact with the overlying silt. d13C, d18O and D47 measurements of carbonate were made using an automated common acid bath peripheral coupled to a Thermo MAT 253 mass spectrometer at Johns Hopkins University, using methods described previously27. The results are reported in Supplementary Table 8. 28. Kuiper, K. F. et al. Synchronizing rock clocks of earth history. Science 320, 500–504 (2008). RESEARCH ARTICLE ©2012 Macmillan Publishers Limited. All rights reserved