Among extant hominoids, modern humans (Homo sapiens; hereafter, ‘humans’) are the only habitually bipedal species. Adaptation to upright walking and running in humans is evidenced by the presence of a host of postcranial morphologies functionally related to saving mechanical and metabolic energy (Lovejoy, 1988; Bramble and Lieberman, 2004; Pontzer, 2017). These include relatively long legs, arched feet (Venkadesan et al., 2020), and adaptations to protect the joints of the lower limbs from excessive stress by increasing their surface areas relative to the mass of the body (Ruff, 1988; Jungers, 1988; Lovejoy, 2005). These morphological traits are most strongly expressed in recent modern humans, which are nearly exclusively terrestrial in their locomotor adaptation. In contrast, the body plan of extant, nonhuman apes (hereafter, simply ‘apes’) reflects an adaptation to orthogrady and suspension (Keith, 1923; Gebo, 1996; Williams and Russo, 2015) with relatively long arms and large upper limb joints (Ruff, 1988), elongated, curved phalanges (Deane and Begun, 2008), and other morphological features suitable for arboreal behaviors (Gebo, 1996). Although chimpanzees, bonobos, and gorillas possess adaptations to terrestrial quadrupedalism (Gebo, 1996), including their knuckle-walking hand posture and heel-strike plantigrade foot posture (Gebo, 1992; Prang, 2019), they retain traits linked to an ancestry characterized by vertical climbing and suspension in some form (Gebo, 1996).

The relatively larger upper limb joints of apes compared to humans reflect disparate joint loading regimes associated with forms of quadrupedalism, climbing, and suspension (Gebo, 1996). Additionally, the relatively larger surface areas of the convex side of conarticular joints may contribute to increased range of motion, providing benefits to the arboreal locomotor performance of apes (Ruff, 1988; Godfrey et al., 1991; Hammond, 2014; Prang, 2016). Therefore, the relative size of postcranial joints and the relationship between the joints of the upper and lower limbs are important correlates of positional and locomotor behavior among hominoids (Ruff, 1988; Jungers, 1988; Godfrey et al., 1995; McHenry, 1992; McHenry and Berger, 1998; Green et al., 2007; Haeusler and McHenry, 2007).

The timing and pattern of the complicated, nonlinear evolutionary loss of adaptations to arboreality and the transition to a form of nearly exclusive terrestrial bipedalism among hominins has been debated for decades (Stern, 2000; Ward, 2002). The study of limb joint proportions initially focused on the preserved partial skeletons A.L. 288-1 (Australopithecus afarensis) and StW 431 (Australopithecus africanus) (McHenry and Berger, 1998; Green et al., 2007), along with OH 62 and KNM-ER 3735 (Homo habilis; Haeusler and McHenry, 2007; Johanson et al., 1987; Leakey et al., 1987). Previous studies have shown that the geologically younger A. africanus possessed relatively large upper limb joints and metaphyseal dimensions in comparison to A. afarensis (McHenry and Berger, 1998; Green et al., 2007). The OH 62 and KNM-ER 3735 partial skeletons are more fragmentary, but morphological comparisons of external morphology (Haeusler and McHenry, 2007; Hartwig-Scherer and Martin, 1991) and cross-sectional geometry (Ruff, 2009) suggest that the upper limbs of H. habilis bore similarities to extant chimpanzees and gorillas, implying greater reliance on forelimb-dominated behaviors, and may show a similar pattern to that observed in A. africanus (McHenry and Berger, 1998; Green et al., 2007; Haeusler and McHenry, 2007). The observed pattern of joint size proportions among extant hominoids implies that the relatively larger lower limb joints of A. afarensis are a reflection of increased terrestriality compared to A. africanus.

Cladistic analyses of hominin phylogeny based on craniodental characters consistently position A. africanus as more closely related to Homo than is A. afarensis (Dembo et al., 2016; Strait et al., 2015). Therefore, either (1) A. afarensis and H. sapiens independently evolved relatively larger lower limb joints (i.e., their similarities are homoplastic), (2) A. africanus and H. habilis evolved more ape-like joint proportions from an ancestor with more human-like limb proportions (i.e., the similarities between A. africanus, H. habilis, and apes are homoplastic), or (3) A. afarensis is more closely related to Homo than are A. africanus and H. habilis (Figure 1). Limited taxonomic sampling of fossil hominins in previous studies has rendered these competing scenarios exceedingly difficult to differentiate. Over the past few decades, however, the recovery of new fossil hominin partial skeletons preserving both upper and lower limb joints has provided an expanded sample that can be used to evaluate these hypotheses more rigorously (Table 1). Here, we re-examine the upper and lower limb joint proportions of multiple species of Australopithecus, Paranthropus, and Homo to evaluate these long-standing alternative hypotheses for patterns of postcranial evolution in hominins.

Figure 1

Download asset Open asset

We quantified limb joint proportions per individual using the relative limb size index (RLSI) (Green et al., 2007). The RLSI is the logged ratio of geometric means calculated from upper (forelimb) and lower (hindlimb) limb measurements and quantifies whether a given specimen has relatively larger forelimb or hindlimb joints (Green et al., 2007). We calculated a series of RLSIs to accommodate the differential preservation of postcranial elements among the 16 hominin partial skeletons sampled here. When the full upper to lower limb dataset is used, there is clear separation between humans, with their proportionally larger lower limbs, and modern apes, with their proportionately larger upper limbs, with no overlap. Importantly, there remains clear separation between humans and great apes in cases where truncated datasets were used to quantify the limb joint proportions of less complete hominin skeletons. The ape data, however, do not always accord with degree of arboreality (hylobatid > Pongo > Pan > Gorilla).

5 of the 16 partial hominin skeletons are human-like in their limb joint proportions (Figure 2, Figure 2—figure supplements 1–26). The RLSI of A.L. 288-1 (Lucy) is far outside the ape range and falls squarely within the range of modern humans (Figure 2, Figure 2—figure supplement 1). Likewise, the larger, presumed male A. afarensis partial skeleton KSD-VP-1/1 is positioned within the human range, though it overlaps with the low end of the hylobatid distribution (Figure 2—figure supplement 2). The infant partial skeleton of A. afarensis (DIK-1-1), as well as Lucy, has a human-like glenoid:talus ratio (Figure 2—figure supplement 3). KNM-WT 15000 (Homo erectus) has even larger relative lower limb joint proportions than the humans sampled in this study and is well outside the ape range (Figure 2—figure supplement 4). LES 1 (Homo naledi) falls within the human interquartile range, outside any modern ape distribution (Figure 2—figure supplement 5).

Figure 2 with 26 supplements see all

Download asset Open asset

Figure 2—source data 1

Raw measurements on extant primate skeletons.

https://cdn.elifesciences.org/articles/65897/elife-65897-fig2-data2-v1.xlsx

Download elife-65897-fig2-data2-v1.xlsx

All of the other hominin skeletons studied fall outside the human range, indicating that they are more ape-like in their joint proportions (Figure 2). StW 431 (A. africanus) has limb proportions positioned within the hylobatid interquartile range and within the distributions of Pan, Gorilla, and Pongo (Figure 2—figure supplement 6). MH1 (juvenile Australopithecus sediba) falls within the interquartile range of hylobatids and Pan and within the ranges of Gorilla and Pongo (Figure 2—figure supplement 7). MH2 (adult A. sediba) occupies the space between great apes and humans, positioned only within the range of hylobatids (Figure 2—figure supplement 8). StW 573 is similar to MH2 in having relatively larger upper limb joints than modern humans but smaller than extant apes, positioned only near a hylobatid outlier (Figure 2—figure supplement 9).

Partial skeletons attributed to Paranthropus all possess ape-like joint proportions. TM 1517 (Paranthropus robustus) and KNM-ER 1500 (Paranthropus boisei) fall within the ranges of all four extant apes (Figure 2—figure supplements 10 and 11). OH 80 (P. boisei) falls within the interquartile range of Pan and the range of Gorilla and hylobatids (Figure 2—figure supplement 12). Associated fossils KNM-ER 1503/1504 (tentatively attributed to P. boisei) have joint proportions within the interquartile range of Pan, Gorilla, and hylobatids (Figure 2—figure supplement 13).

BOU-VP-12/1 (Australopithecus cf. garhi) falls squarely within the Gorilla interquartile range and within the lower range of Pan (Figure 2—figure supplement 14). There is a single human outlier overlapping with the limb joint proportions of BOU-VP-12/1.

KNM-ER 3735 (H. habilis) has joint proportions in the hylobatid interquartile range and within the ranges of all extant great apes (Figure 2—figure supplement 15). The joint proportions of LB 1 (Homo floresiensis) fall within the ranges for all of the apes, though there is a single human outlier similar in joint proportions to LB 1 (Figure 2—figure supplement 16).

Parsimony reconstructions suggest that the human-like limb joint proportions in A. afarensis and modern humans are homoplastic, regardless of the phylogenetic hypothesis used (Figure 3). The only phylogenetic hypothesis that does not require either homoplasy or multiple reversals is one in which A. afarensis is more derived than H. habilis, H. floresiensis, and all other species of Australopithecus and Paranthropus examined in this study. Given that an A. afarensis-later Homo clade (to the exclusion of early Homo) has not been supported by any phylogenetic analysis, we consider this last scenario unlikely in the extreme.

Figure 3

Download asset Open asset

Apes have relatively larger upper limb than lower limb joints as reflected by their higher RLSI than modern humans (Green et al., 2007). With musculoskeletal anatomies adapted for climbing and suspension, apes possess larger upper limb muscles and joints with greater surface areas, which has the effect of limiting excessive stresses and strains arising from large joint reaction forces. Enlarged upper limb joint surface areas in apes may also contribute to increased ranges of motion (e.g., at the glenohumeral joint). In contrast, humans are characterized by relatively larger lower limb joints, which act to reduce stresses and strains on the joints and nonrenewable cartilage of the hip, knee, and ankle arising from repetitive high-magnitude ground and joint reaction forces during heel-striking bipedal walking and running. This pattern accords with expectations based on the posture and locomotion of apes and humans. Apes possess heavily built upper limbs associated with orthograde climbing and suspension, whereas modern humans have robust lower limbs adapted to terrestrial bipedalism. This morphological pattern provides a framework for interpreting the functional and evolutionary implications of joint proportions in fossil hominins.

It is noteworthy, however, that the ape RLSI did not always align with degree of arboreality (hylobatid > Pongo > Pan > Gorilla). As reported elsewhere (Gordon et al., 2020), the preserved anatomical elements used to calculate RLSI can impact where a taxon is positioned along a locomotor continuum. The relatively narrow great ape sacrum, hypothesized to facilitate entrapment of the lumbar vertebrae and stiffen the lower back during climbing, further increases the RLSI of Pan, Gorilla, and Pongo relative to the hylobatids (Figure 4—figure supplements 1–4). Additionally, while RLSI calculations that included the radial head and ulnar trochlear width separate the ape species by locomotor mode, those that include the glenoid size and the biepicondylar breadth do not. In fact, a post hoc examination of limb joint scaling found that while great apes and humans exhibit isometric scaling of the glenoid and humeral biepicondylar breadth relative to femoral head diameter, the hylobatids scale with negative allometry (glenoid m = 0.75; biepicondylar breadth m = 0.76). It is likely that the differing sizes of these apes and the functional demands on the limb joints in arboreal apes across this size range are driving some of the unexpected RLSI results reported here.

Our study provides a fresh perspective on alternative hypotheses for the evolution of limb joint proportions introduced by previous workers (McHenry and Berger, 1998; Green et al., 2007; Haeusler and McHenry, 2007). The reconstruction of patterns of hominin evolution relies on phylogeny, and, since the early adoption of cladistics, no quantitative analysis of hominin phylogeny has recovered a sister taxon relationship between A. afarensis and Homo (Dembo et al., 2016; Strait et al., 2015). The recovery of purported Homo fossils significantly predating the appearance of A. africanus and A. sediba may falsify hypotheses of exclusive ancestry and descent (Du and Alemseged, 2019). However, the consistent placement of A. africanus and A. sediba near Homo implies that they share a more recent common ancestor than do Homo and A. afarensis, despite their temporal and geographic distance (Dembo et al., 2016; Berger et al., 2010; Irish et al., 2013; Pickering et al., 2011). The inclusion of Paranthropus and early Homo fossils here helps alleviate the evolutionary implications of uncertainty surrounding the phylogenetic positions of Australopithecus species. The homology of a low RLSI in A. afarensis and later Homo can only be explained by an increasingly large number of evolutionary reversals. The independent evolution of similar limb joint proportions in A. afarensis and later Homo is a more parsimonious interpretation of the data.

There exists one additional piece of evidence that supports our interpretation that the low RLSI of A. afarensis and modern humans is homoplastic. Interestingly, the low RLSI of A. afarensis was achieved with a different morphological pattern compared to H. erectus. We found that H. erectus possessed a relatively smaller sacral body (like A. africanus and A. sediba) but a large femoral head relative to the upper limb than do modern humans; however, A. afarensis possessed a relatively small femoral head and large sacral body (Figure 4). This finding may further imply parallel evolution in limb joint proportions between A. afarensis and H. sapiens. The relatively small sacral body of the female H. erectus sacrum from Gona (Simpson et al., 2008, personal observation) demonstrates that these results are not the result of the juvenile status of KNM-WT 15000.

Figure 4 with 4 supplements see all

Download asset Open asset

The morphology and functional anatomy of the axial skeleton, pelvis, and lower limb display unambiguous evidence for bipedal posture and locomotion in Australopithecus and later hominins. Furthermore, the presence of traits potentially signifying the importance of arboreality among fossil hominins does not necessarily imply reduced bipedal competency. However, the distributions of RLSI data (Figure 2—figure supplements 17–26), along with observations of other regional anatomies, imply differences among hominins in their adaptation to terrestrial, heel-striking bipedality. A. afarensis has relatively larger lower limb joints than any other early hominin currently known and possesses features of the foot and ankle that imply bipedal performance capabilities exceeding those of later early hominins. These traits include a more robust calcaneal tuber, a flatter subtalar joint, and a more plantarly oriented fourth metatarsal diaphysis and talonavicular joint (reviewed in DeSilva et al., 2019). The available morphological evidence suggests that, compared to other Plio-Pleistocene hominins, A. afarensis was better able to withstand the stresses and strains induced by the repetitive loading of the lower limb in frequent terrestrial bipedalism.

Over the past three decades, significant emphasis has been placed on the retention of ape-like characters in Australopithecus and Paranthropus since they could have been maintained through stabilizing selection if arboreality was a significant part of their positional repertoires (Stern, 2000). However, many researchers have repeatedly noted the difficulty of distinguishing the effects of stabilizing selection from those of evolutionary inertia (or ‘lag’). This critique is rooted in a maximum likelihood, character-based cladistic framework, which implicitly excludes information about the evolutionary process (e.g., evolutionary rates as a function of time). In other words, primitive retentions have the same meaning across varying temporal ranges in a traditional cladistic framework. The presence of presumed primitive, ape-like features in late Australopithecus and early Homo c. ~2 Ma implies that evolutionary processes, whether neutral (i.e., genetic drift) or non-neutral (i.e., directional selection), had not yet substantially modified them over a 4- to 5 million-year period given current estimates of the Pan-Homo divergence date. Therefore, in our view, primitive retentions in Australopithecus, Paranthropus, and Homo can be meaningful when interpreted within the context of the evolutionary process.

Regardless of assumptions underlying evolutionary processes, primitive retentions in late Australopithecus and early Homo occur alongside indirect evidence for arboreal activity in their trabecular bone density patterns and long bone diaphyseal properties. A recent study of trabecular bone density of the non-pollical metacarpal heads of A. sediba showed a close morphometric affinity with extant orangutans, despite having human-like hand proportions (Dunmore et al., 2020). The external structure and internal trabecular morphology of the A. sediba hand are consistent with the use of forceful metacarpophalangeal joint flexion, which is a requisite of forelimb-dominated, below-branch locomotion (Dunmore et al., 2020). The purportedly more ape-like limb joint and length proportions of the OH 62 partial skeleton are supported by a more chimpanzee-like humeral cross-sectional geometry, implying that the H. habilis upper limb was heavily built (Ruff, 2009). The femoral head trabecular bone density pattern of StW 311 from Sterkfontein attributed either to P. robustus or Homo sp. implies the more habitual use of flexed hip postures, which occurs during climbing (Georgiou et al., 2020).

In light of the congruence between the functional interpretations derived from the external and internal morphology of hominin postcranial fossils, we consider the limb joint proportions data presented here, and in previous studies, to be a reliable indicator of adaptation to arboreal locomotion. The relatively larger hindlimb joints of A. afarensis and later Homo are consistent with a more pronounced terrestrial component of their positional repertoires, whereas the relatively larger upper limb joints of most Australopithecus, Paranthropus, and early Homo individuals indicate a more pronounced arboreal component. The low RLSI of A. afarensis does not imply a lack of arboreal activity given the evidence it climbed trees (Stern and Susman, 1983; Ruff et al., 2016; Green and Alemseged, 2012; DeSilva et al., 2018b). The glenoid:talus proportions of the DIK-1-1 juvenile are human-like and distinct from this ratio in modern apes or in other species of Australopithecus, despite the presence of a Gorilla-like scapula (Green and Alemseged, 2012) and medial cuneiform (DeSilva et al., 2018b) indicating increased arboreal competency among juveniles. Furthermore, although A. afarensis had a more modern human-like RLSI, it possessed relatively longer arms and shorter legs than modern humans (Holliday, 2012), with more chimpanzee-like humeral-femoral strength proportions (Ruff et al., 2016), suggesting that the body plan and positional repertoire of A. afarensis were unique and unlike any living taxon.

We acknowledge that one of the limitations of our study includes uncertainty surrounding the taxonomic affinity of partial skeletons such as KNM-ER 1500. However, our evolutionary interpretation would not be altered by accepting the alternative interpretation of KNM-ER 1500 as H. habilis. Our finding that Paranthropus had a high RLSI is consistent with recent evidence suggesting the presence of heavily built, somewhat ape-like, distal humeri in this genus (Lague et al., 2019). Additionally, for some specimens (e.g. KNM-ER 1503/1504, TM 1517), uncertainty remains about whether they represent a single partial skeleton, but recent work supports the single-individual hypothesis for TM 1517 (Cazenave et al., 2020). Finally, two skeletons used in this study are juveniles (MH1 and KNM-WT 15000), though they are near skeletal maturation. Despite their juvenile status, MH1 has more ape-like limb joint proportions, whereas KNM-WT 15000 is more modern human-like. Fortunately, the limb joint proportions of A. sediba are represented by the MH2 adult specimen. A future study could evaluate the relative size and ontogenetic scaling of limb joint proportions across hominoids to evaluate the morphometric and functional affinities of juvenile hominin specimens in greater detail (e.g., DIK-1-1).

Despite these minor caveats, the pattern of limb joint proportions in hominins is clear. Partial skeletons belonging to A. afarensis, H. erectus, and H. naledi are human-like, with a low RLSI, whereas all others are more ape-like, with a high RLSI. These data strongly suggest that A. afarensis was a committed terrestrial biped that evolved adaptations to limit the larger lower limb stresses and strains characteristic of bipedal locomotion, as also occurred in later Pleistocene Homo (but not H. floresiensis). Other species of Australopithecus, Paranthropus, and early members of the genus Homo appear to have been less committed terrestrial bipeds that retained adaptations to the arboreal milieu. Overall, our analysis provides resolution on a long-standing hypothesis that A. afarensis evolved its low RLSI independently of some later Pleistocene hominins.

The comparative sample includes hylobatids (all four genera are represented, total N = 69; Hoolock: N = 11; Hylobates: N = 39; Nomascus: N = 5; Symphalangus: N = 14), Pongo spp. (total N = 50; Pongo abelii: N = 13; Pongo pygmaeus, N = 37), Gorilla spp. (total N = 131; Gorilla beringei: 55; Gorilla gorilla: N = 76), Pan spp. (total N = 124; Pan paniscus: N = 26, Pan troglodytes: N = 98), and H. sapiens (N = 67). We measured adult specimens from the Harvard Museum of Comparative Zoology, the American Museum of Natural History, and the Cleveland Museum of Natural History. Data for hominin partial skeletons (N = 16) were acquired from published literature and/or measured on original fossils using Mitutoyo calipers. In some cases, casts from the Dartmouth Paleoanthropology lab were used to confirm published measurements.

Seven measurements were taken at the shoulder and elbow joints to represent the upper body (Figure 5): scapular glenoid superoinferior (SI) height and maximum mediolateral (ML) width, humeral head SI height and anteroposterior (AP) width, humeral biepicondylar breadth, ulnar olecranon width, and radial head semimajor axis diameter. Seven measurements were taken at the hip, lumbosacral, and talocrural joints to represent the lower body (Figure 5): acetabulum SI height, SI femoral head diameter, femoral subtrochanteric ML width and AP breadth, sacral (S1) body maximum ML width and AP diameter at midline, and width of the talar trochlear apex taken at the midpoint. Mean scapular glenoid and humeral head joint size was calculated using a geometric mean of the SI and ML dimensions. Mean femoral subtrochanteric and sacral body size was calculated using a geometric mean of the AP and ML dimensions.

Figure 5

Download asset Open asset

We quantified limb joint proportions per individual using the RLSI (Green et al., 2007). The RLSI is the logged ratio of geometric means calculated from forelimb and hindlimb measurements (Green et al., 2007). Geometric means are typically used as size proxies over arithmetic means because they accommodate measurements with different ranges, which is common for morphometric measurements, and therefore normalize the weight of individual measurements (Jungers et al., 1995). Logging the ratio is necessary because ratios of normally distributed data cannot be normally distributed and thus violate the assumptions of statistical tests (e.g., Green et al., 2007; Smith, 1999). The measurements used to calculate the limb joint proportions of hominin specimens varied depending on which measurements were preserved in the fossil (Supplementary file 1). Separate comparative analyses including different ratios were conducted for each hominin partial skeleton to maximize the fossil sample.

To visualize evolutionary scenarios, we conducted ancestral states using parsimony on a variety of phylogenetic hypotheses. These hypotheses included both formal cladistic analyses (Dembo et al., 2016; Strait et al., 2015; Mongle et al., 2019) and published hypotheses that have not been recovered in phylogenetic analyses (Asfaw et al., 1999; Wood and Schroer, 2017; Villmoare, 2018).

All data generated during this study are included in the manuscript (Table 1). Raw data from extant specimens appears as an Excel file in Figure 2-source data 1.

1. 1. Asfaw B
   2. White T
   3. Lovejoy O
   4. Latimer B
   5. Simpson S
   6. Suwa G

   (1999) Australopithecus garhi: a new species of early hominid from Ethiopia

   Science 284:629–635.

   https://doi.org/10.1126/science.284.5414.629

   • PubMed
   • Google Scholar
2. 1. Berger LR
   2. de Ruiter DJ
   3. Churchill SE
   4. Schmid P
   5. Carlson KJ
   6. Dirks P
   7. Kibii JM

   (2010) Australopithecus sediba: a new species of Homo-like australopith from South Africa

   Science 328:195–204.

   https://doi.org/10.1126/science.1184944

   • PubMed
   • Google Scholar
3. 1. Bramble DM
   2. Lieberman DE

   (2004) Endurance running and the evolution of Homo

   Nature 432:345–352.

   https://doi.org/10.1038/nature03052

   • PubMed
   • Google Scholar
4. 1. Cazenave M
   2. Dean C
   3. Zanolli C
   4. Oettlé AC
   5. Hoffman J
   6. Tawane M
   7. Thackeray F
   8. Macchiarelli R

   (2020) Reassessment of the TM 1517 odonto-postcranial assemblage from Kromdraai B, South Africa, and the maturational pattern of Paranthropus robustus

   American Journal of Physical Anthropology 172:714–722.

   https://doi.org/10.1002/ajpa.24082

   • PubMed
   • Google Scholar
5. 1. Churchill SE
   2. Green DJ
   3. Feuerriegel EM
   4. Macias ME
   5. Mathews S
   6. Carlson KJ
   7. Schmid P
   8. Berger LR

   (2019) The shoulder, arm, and forearm of Australopithecus sediba

   PaleoAnthropology.

   https://doi.org/10.4207/PA.2018.ART114

   • Google Scholar
6. 1. Day MH

   (1973)

   Locomotor features of the lower limb in hominids

   Symp Zool Soc Lond 33:29–51.

   • Google Scholar
7. 1. Day MH
   2. Leakey REF
   3. Walker AC
   4. Wood BA

   (1976) New hominids from East Turkana, Kenya

   American Journal of Physical Anthropology 45:369–435.

   https://doi.org/10.1002/ajpa.1330450304

   • PubMed
   • Google Scholar
8. 1. Day MH
   2. Thornton CMB

   (1986)

   The extremity bones of Paranthropus robustus from Kromdraai B, East formation member 3, Republic of South Africa: a reappraisal

   Anthropos 23:91–99.

   • Google Scholar
9. 1. Deane AS
   2. Begun DR

   (2008) Broken fingers: retesting locomotor hypotheses for fossil hominoids using fragmentary proximal phalanges and high-resolution polynomial curve fitting (HR-PCF

   Journal of Human Evolution 55:691–701.

   https://doi.org/10.1016/j.jhevol.2008.05.005

   • PubMed
   • Google Scholar
10. Book

    1. DeGusta DA

    (2004)

    Pliocene Hominid Postcranial Fossils from the Middle Awash, Ethiopia

    Berkeley: University of California.

    • Google Scholar
11. 1. Dembo M
    2. Radovčić D
    3. Garvin HM
    4. Laird MF
    5. Schroeder L
    6. Scott JE
    7. Brophy J
    8. Ackermann RR
    9. Musiba CM
    10. de Ruiter DJ
    11. Mooers AØ
    12. Collard M

    (2016) The evolutionary relationships and age of Homo naledi: An assessment using dated bayesian phylogenetic methods

    Journal of Human Evolution 97:17–26.

    https://doi.org/10.1016/j.jhevol.2016.04.008

    • PubMed
    • Google Scholar
12. 1. DeSilva JM

    (2011) A shift toward birthing relatively large infants early in human evolution

    PNAS 108:1022–1027.

    https://doi.org/10.1073/pnas.1003865108

    • Google Scholar
13. 1. DeSilva JM
    2. Carlson KJ
    3. Claxton A
    4. Harcourt-Smith WEH
    5. McNutt E
    6. Sylvester AD
    7. Walker C
    8. Zipfel B
    9. Churchill SE
    10. Berger LR

    (2018a) The anatomy of the lower limb skeleton of Australopithecus sediba

    PaleoAnthropology.

    https://doi.org/10.4207/PA.2018.ART117

    • Google Scholar
14. 1. DeSilva JM
    2. Gill CM
    3. Prang TC
    4. Bredella MA
    5. Alemseged Z

    (2018b) A nearly complete foot from Dikika, Ethiopia and its implications for the ontogeny and function of Australopithecus afarensis

    Science Advances 4:eaar7723.

    https://doi.org/10.1126/sciadv.aar7723

    • PubMed
    • Google Scholar
15. 1. DeSilva J
    2. McNutt E
    3. Benoit J
    4. Zipfel B

    (2019) One small step: a review of Plio‐Pleistocene hominin foot evolution

    American Journal of Physical Anthropology 168:63–140.

    https://doi.org/10.1002/ajpa.23750

    • Google Scholar
16. 1. Domínguez-Rodrigo M
    2. Pickering TR
    3. Baquedano E
    4. Mabulla A
    5. Mark DF
    6. Musiba C

    (2013) First Partial Skeleton of a 1.34-Million-Year-Old Paranthropus boisei from Bed II, Olduvai Gorge, Tanzania

    PLOS ONE 8:e80347.

    https://doi.org/10.1371/journal.pone.0080347

    • PubMed
    • Google Scholar
17. 1. Du A
    2. Alemseged Z

    (2019) Temporal evidence shows Australopithecus sediba is unlikely to be the ancestor of Homo

    Science Advances 5:eaav9038.

    https://doi.org/10.1126/sciadv.aav9038

    • PubMed
    • Google Scholar
18. 1. Dunmore CJ
    2. Skinner MM
    3. Bardo A
    4. Berger LR
    5. Hublin J-J
    6. Pahr DH
    7. Rosas A
    8. Stephens NB
    9. Kivell TL

    (2020) The position of Australopithecus sediba within fossil hominin hand use diversity

    Nature Ecology & Evolution 4:911–918.

    https://doi.org/10.1038/s41559-020-1207-5

    • Google Scholar
19. 1. Feuerriegel EM
    2. Voisin JL
    3. Churchill SE
    4. Häusler M
    5. Mathews S
    6. Schmid P
    7. Hawks J
    8. Berger LR

    (2019) Upper limb fossils of Homo naledi from the lesedi chamber, rising Star System, South Africa

    PaleoAnthropology pp. 311–349.

    https://doi.org/10.4207/PA.2019.ART134

    • Google Scholar
20. 1. Gebo DL

    (1992) Plantigrady and foot adaptation in african apes: Implications for hominid origins

    American Journal of Physical Anthropology 89:29–58.

    https://doi.org/10.1002/ajpa.1330890105

    • PubMed
    • Google Scholar
21. 1. Gebo DL

    (1996) Climbing, brachiation, and terrestrial quadrupedalism: Historical precursors of hominid bipedalism

    American Journal of Physical Anthropology 101:55–92.

    https://doi.org/10.1002/(SICI)1096-8644(199609)101:1<55::AID-AJPA5>3.0.CO;2-C

    • PubMed
    • Google Scholar
22. 1. Georgiou L
    2. Dunmore CJ
    3. Bardo A
    4. Buck LT
    5. Hublin J-J
    6. Pahr DH
    7. Stratford D
    8. Synek A
    9. Kivell TL
    10. Skinner MM

    (2020) Evidence for habitual climbing in a Pleistocene hominin in South Africa

    PNAS 117:8416–8423.

    https://doi.org/10.1073/pnas.1914481117

    • Google Scholar
23. 1. Godfrey L
    2. Sutherland M
    3. Boy D
    4. Gomberg N

    (1991) Scaling of limb joint surface areas in anthropoid primates and other mammals

    Journal of Zoology 223:603–625.

    https://doi.org/10.1111/j.1469-7998.1991.tb04391.x

    • Google Scholar
24. 1. Godfrey LR
    2. Sutherland MR
    3. Paine RR
    4. Williams FL
    5. Boy DS
    6. Vuillaume‐Randriamanantena M

    (1995) Limb joint surface areas and their ratios in malagasy lemurs and other mammals

    American Journal of Physical Anthropology 97:11–36.

    https://doi.org/10.1002/ajpa.1330970103

    • Google Scholar
25. Book

    1. Gordon AD
    2. Green DJ
    3. Jungers WL
    4. Richmond BG

    (2020) Limb proportions and positional behavior: Revisiting the theoretical and empirical underpinnings for locomotor reconstruction in Australopithecus africanus

    In: Zipfel B, Richmond BG, Ward CV, editors. Hominid Postcranial Remains from Sterkfontein, South Africa, 1936-1995. Advances in Human Evolution Series. Oxford, United Kingdom: Oxford University Press. pp. 321–334.

    https://doi.org/10.1093/oso/9780197507667.001.0001

    • Google Scholar
26. Book

    1. Grausz HM
    2. Leakey REF
    3. Walker AC
    4. Ward CV

    (1988)

    Associated cranial and postcranial bones of Australopithecus boisei

    In: Grine FE, editors. Evolutionary History of the ‘“Robust”’ Australopithecines. Aldine de Gruyter. pp. 127–132.

    • Google Scholar
27. 1. Green DJ
    2. Gordon AD
    3. Richmond BG

    (2007) Limb-size proportions in Australopithecus afarensis and Australopithecus africanus

    Journal of Human Evolution 52:187–200.

    https://doi.org/10.1016/j.jhevol.2006.09.001

    • PubMed
    • Google Scholar
28. 1. Green DJ
    2. Alemseged Z

    (2012) Australopithecus afarensis scapular ontogeny, function, and the role of climbing in human evolution

    Science 338:514–517.

    https://doi.org/10.1126/science.1227123

    • PubMed
    • Google Scholar
29. 1. Haeusler M
    2. McHenry HM

    (2007) Evolutionary reversals of limb proportions in early hominids? Evidence from KNM-ER 3735 (Homo habilis

    Journal of Human Evolution 53:383–405.

    https://doi.org/10.1016/j.jhevol.2007.06.001

    • PubMed
    • Google Scholar
30. 1. Haile-Selassie Y
    2. Latimer BM
    3. Alene M
    4. Deino AL
    5. Gibert L
    6. Melillo SM
    7. Saylor BZ
    8. Scott GR
    9. Lovejoy CO

    (2010) An early Australopithecus afarensis postcranium from Woranso-Mille, Ethiopia

    PNAS 107:12121–12126.

    https://doi.org/10.1073/pnas.1004527107

    • Google Scholar
31. Book

    1. Haile-Selassie Y
    2. Su DF

    (2015) The Postcranial Anatomy of Australopithecus afarensis: New Insights from KSD-VP-1/1

    Springer.

    https://doi.org/10.1007/978-94-017-7429-1

    • Google Scholar
32. 1. Hammond AS

    (2014) In vivo baseline measurements of hip joint range of motion in suspensory and nonsuspensory anthropoids

    American Journal of Physical Anthropology 153:417–434.

    https://doi.org/10.1002/ajpa.22440

    • PubMed
    • Google Scholar
33. 1. Hartwig-Scherer S
    2. Martin RD

    (1991) Was “Lucy” more human than her “child”? Observations on early hominid postcranial skeletons

    Journal of Human Evolution 21:439–449.

    https://doi.org/10.1016/0047-2484(91)90094-C

    • Google Scholar
34. 1. Hawks J
    2. Elliot M
    3. Schmid P
    4. Churchill SE
    5. de Ruiter DJ
    6. Roberts E
    7. Hilbert-Wolf H
    8. Garvin HM
    9. Williams SA
    10. Delezene LK
    11. Feuerriegel EM
    12. Randolph-Quinney P
    13. Kivell TL
    14. DeSilva JM
    15. Bailey SE
    16. Brophy JK
    17. Meyer MR
    18. Skinner MM
    19. Tocheri MW
    20. VanSickle C
    21. Walker CS
    22. Campbell TL
    23. Kuhn B
    24. Kruger A
    25. Tucker S
    26. Gurtov A
    27. Hlophe N
    28. Hunter R
    29. Morris H
    30. van Rooyen D
    31. Tsikoane M
    32. Dirks P
    33. Berger LR

    (2017) New fossil remains of Homo naledi from the Lesedi chamber South Africa

    eLife 6:e24232.

    https://doi.org/10.7554/eLife.24232

    • Google Scholar
35. 1. Heaton JL
    2. Pickering TR
    3. Carlson KJ
    4. Crompton RH
    5. Jashashvili T
    6. Beaudet A
    7. Bruxelles L
    8. Kuman K
    9. Heile AJ
    10. Stratford D
    11. Clarke RJ

    (2019) The long limb bones of the StW 573 Australopithecus skeleton from Sterkfontein Member 2: Descriptions and proportions

    Journal of Human Evolution 133:167–197.

    https://doi.org/10.1016/j.jhevol.2019.05.015

    • PubMed
    • Google Scholar
36. 1. Holliday TW

    (2012) Body size, body shape, and the circumscription of the genus Homo

    Current Anthropology 53:S330–S345.

    https://doi.org/10.1086/667360

    • Google Scholar
37. 1. Irish JD
    2. Guatelli-Steinberg D
    3. Legge SS
    4. de Ruiter DJ
    5. Berger LR

    (2013) Dental morphology and the phylogenetic “place” of Australopithecus sediba

    Science 340:1233062.

    https://doi.org/10.1126/science.1233062

    • PubMed
    • Google Scholar
38. 1. Johanson DC
    2. Lovejoy CO
    3. Kimbel WH
    4. White TD
    5. Ward SC
    6. Bush ME
    7. Latimer BM
    8. Coppens Y

    (1982) Morphology of the Pliocene partial hominid skeleton (A.L. 288-1) from the Hadar formation, Ethiopia

    American Journal of Physical Anthropology 57:403–451.

    https://doi.org/10.1002/ajpa.1330570403

    • Google Scholar
39. 1. Johanson DC
    2. Masao FT
    3. Eck GG
    4. White TD
    5. Walter RC
    6. Kimbel WH
    7. Asfaw B
    8. Manega P
    9. Ndessokia P
    10. Suwa G

    (1987) New partial skeleton of Homo habilis from Olduvai Gorge, Tanzania

    Nature 327:205–209.

    https://doi.org/10.1038/327205a0

    • PubMed
    • Google Scholar
40. 1. Jungers WL

    (1988) Relative joint size and hominoid locomotor adaptations with implications for the evolution of hominid bipedalism

    Journal of Human Evolution 17:247–265.

    https://doi.org/10.1016/0047-2484(88)90056-5

    • Google Scholar
41. 1. Jungers WL
    2. Falsetti AB
    3. Wall CE

    (1995) Shape, relative size, and size-adjustments in morphometrics

    American Journal of Physical Anthropology 38:137–161.

    https://doi.org/10.1002/ajpa.1330380608

    • Google Scholar
42. 1. Jungers WL
    2. Larson SG
    3. Harcourt-Smith W
    4. Morwood MJ
    5. Sutikna T
    6. Due Awe R
    7. Djubiantono T

    (2009) Descriptions of the lower limb skeleton of Homo floresiensis

    Journal of Human Evolution 57:538–554.

    https://doi.org/10.1016/j.jhevol.2008.08.014

    • Google Scholar
43. 1. Keith A

    (1923) Man’s posture: Its evolution and disorders

    Am J Pub Health 13:580.

    https://doi.org/10.2105/ajph.13.7.580

    • Google Scholar
44. 1. Lague MR
    2. Chirchir H
    3. Green DJ
    4. Mbua E
    5. Harris JWK
    6. Braun DR
    7. Griffin NL
    8. Richmond BG

    (2019) Cross-sectional properties of the humeral diaphysis of Paranthropus boisei: Implications for upper limb function

    Journal of Human Evolution 126:51–70.

    https://doi.org/10.1016/j.jhevol.2018.05.002

    • PubMed
    • Google Scholar
45. 1. Larson SG
    2. Jungers WL
    3. Tocheri TM
    4. Orr CM
    5. Morwood MJ
    6. Sutikna T
    7. Awe RD
    8. Djubiantono T

    (2009) Descriptions of the upper limb skeleton of Homo floresiensis

    Journal of Human Evolution 57:555–570.

    https://doi.org/10.1016/j.jhevol.2008.06.007

    • PubMed
    • Google Scholar
46. 1. Leakey REF

    (1973) Further evidence of lower pleistocene hominids from East Rudolf, North Kenya, 1972

    Nature 242:170–173.

    https://doi.org/10.1038/242170a0

    • PubMed
    • Google Scholar
47. Book

    1. Leakey MG
    2. Leakey REF

    (1978)

    The Fossil Hominids and an Introduction to Their Context. 1968-1974

    Oxford: Clarendon.

    • Google Scholar
48. Book

    1. Leakey REF
    2. Walker A
    3. Ward CV
    4. Grausz HM

    (1987)

    A partial skeleton of a gracile hominid from the upper Burgi member of the Koobi Fora formation, East Lake Turkana, Kenya

    In: Giacobini G, editors. Hominidae: Proceedings of the 2nd International Congress of Human Paleontology Turin. Congresso Internazionale. pp. 167–174.

    • Google Scholar
49. 1. Lovejoy CO

    (1988) Evolution of human walking

    Scientific American 259:118–125.

    https://doi.org/10.1038/scientificamerican1188-118

    • PubMed
    • Google Scholar
50. 1. Lovejoy CO

    (2005) The natural history of human gait and posture: Part 2. Hip and thigh

    Gait & Posture 21:113–124.

    https://doi.org/10.1016/j.gaitpost.2004.06.010

    • Google Scholar
51. 1. McHenry HM

    (1992) Body size and proportions in early hominids

    American Journal of Physical Anthropology 87:407–431.

    https://doi.org/10.1002/ajpa.1330870404

    • PubMed
    • Google Scholar
52. 1. McHenry HM
    2. Berger LR

    (1998) Body proportions in Australopithecus afarensis and A. africanus and the origin of the genus Homo

    Journal of Human Evolution 35:1–22.

    https://doi.org/10.1006/jhev.1997.0197

    • PubMed
    • Google Scholar
53. 1. Mongle CS
    2. Strait DS
    3. Grine FE

    (2019) Expanded character sampling underscores phylogenetic stability of Ardipithecus ramidus as a basal hominin

    Journal of Human Evolution 131:28–39.

    https://doi.org/10.1016/j.jhevol.2019.03.006

    • PubMed
    • Google Scholar
54. 1. Pickering R
    2. Dirks P
    3. Jinnah Z
    4. de Ruiter DJ
    5. Churchill SE
    6. Herries AIR
    7. Woodhead JD
    8. Hellstrom JC
    9. Berger LR

    (2011) Australopithecus sediba at 1.977 ma and implications for the origins of the genus Homo

    Science 333:1421–1423.

    https://doi.org/10.1126/science.1203697

    • Google Scholar
55. 1. Pontzer H

    (2017) Economy and endurance in human evolution

    Current Biology 27:R613–R621.

    https://doi.org/10.1016/j.cub.2017.05.031

    • PubMed
    • Google Scholar
56. 1. Prang TC

    (2016) Conarticular congruence of the hominoid subtalar joint complex with implications for joint function in Plio-Pleistocene hominins

    American Journal of Physical Anthropology 160:446–457.

    https://doi.org/10.1002/ajpa.22982

    • PubMed
    • Google Scholar
57. 1. Prang TC

    (2019) The African ape-like foot of Ardipithecus ramidus and its implications for the origin of bipedalism

    eLife 8:e44433.

    https://doi.org/10.7554/eLife.44433

    • PubMed
    • Google Scholar
58. Book

    1. Robinson JT

    (1972)

    Early Hominid Posture and Locomotion

    University of Chicago Press.

    • Google Scholar
59. 1. Ruff C

    (1988) Hindlimb articular surface allometry in Hominoidea and Macaca, with comparisons to diaphyseal scaling

    Journal of Human Evolution 17:687–714.

    https://doi.org/10.1016/0047-2484(88)90025-5

    • Google Scholar
60. 1. Ruff C

    (2009) Relative limb strength and locomotion in Homo habilis

    American Journal of Physical Anthropology 138:90–100.

    https://doi.org/10.1002/ajpa.20907

    • PubMed
    • Google Scholar
61. 1. Ruff CB
    2. Burgess ML
    3. Ketcham RA
    4. Kappelman J

    (2016) Limb bone structural proportions and locomotor behavior in A.L. 288-1 (“Lucy)

    PLOS ONE 11:e0166095.

    https://doi.org/10.1371/journal.pone.0166095

    • PubMed
    • Google Scholar
62. 1. Simpson SW
    2. Quade J
    3. Levin NE
    4. Butler R
    5. Dupont-Nivet G
    6. Everett M
    7. Semaw S

    (2008) A female Homo erectus pelvis from Gona, Ethiopia

    Science 322:1089–1092.

    https://doi.org/10.1126/science.1163592

    • PubMed
    • Google Scholar
63. 1. Smith RJ

    (1999) Statistics of sexual size dimorphism

    Journal of Human Evolution 36:423–458.

    https://doi.org/10.1006/jhev.1998.0281

    • PubMed
    • Google Scholar
64. 1. Stern JT
    2. Susman RL

    (1983) The locomotor anatomy of Australopithecus afarensis

    American Journal of Physical Anthropology 60:279–317.

    https://doi.org/10.1002/ajpa.1330600302

    • PubMed
    • Google Scholar
65. 1. Stern JT

    (2000) Climbing to the top: A personal memoir of Australopithecus afarensis

    Evolutionary Anthropology: Issues, News, and Reviews 9:113–133.

    https://doi.org/10.1002/1520-6505(2000)9:3<113::AID-EVAN2>3.0.CO;2-W

    • Google Scholar
66. Book

    1. Strait DS
    2. Grine FE
    3. Fleagle JG

    (2015) Analyzing hominin phylogeny: Cladistic approach

    In: Henke W, Tattersall I, editors. Handbook of Paleoanthropology. Springer-Verlag. pp. 1989–2014.

    https://doi.org/10.1007/978-3-642-39979-4_58

    • Google Scholar
67. 1. Venkadesan M
    2. Yawar A
    3. Eng CM
    4. Dias MA
    5. Singh DK
    6. Tommasini SM
    7. Haims AH
    8. Bandi MM
    9. Mandre S

    (2020) Stiffness of the human foot and evolution of the transverse arch

    Nature 579:97–100.

    https://doi.org/10.1038/s41586-020-2053-y

    • PubMed
    • Google Scholar
68. 1. Villmoare B

    (2018) Early Homo and the role of the genus in paleoanthropology

    American Journal of Physical Anthropology 165 Suppl 65:72–89.

    https://doi.org/10.1002/ajpa.23387

    • PubMed
    • Google Scholar
69. Book

    1. Walker A
    2. Leakey REF

    (1993)

    The Nariokotome Homo erectus Skeleton

    Berlin, Heidelberg: Harvard University Press.

    • Google Scholar
70. 1. Walker C
    2. Cofran ZD
    3. Grabowski M
    4. Marchi D
    5. Cook RW
    6. Churchill SE
    7. Tommy KA
    8. Throckmorton Z
    9. Ross AH
    10. Hawks J
    11. Yapunich GS
    12. Van Arsdale AP
    13. Rentzeperis F
    14. Berger LR
    15. DeSilva JM

    (2019)

    Morphology and evolution of the Homo naledi femora from Lesedi

    American Journal of Physical Anthropology 170:5–23.

    • Google Scholar
71. 1. Ward CV

    (2002) Interpreting the posture and locomotion of Australopithecus afarensis: Where do we stand?

    American Journal of Physical Anthropology 119:185–215.

    https://doi.org/10.1002/ajpa.10185

    • Google Scholar
72. 1. Williams SA
    2. Russo GA

    (2015) Evolution of the hominoid vertebral column: the long and the short of it

    Evolutionary Anthropology 24:15–32.

    https://doi.org/10.1002/evan.21437

    • PubMed
    • Google Scholar
73. 1. Williams SA
    2. Meyer MR
    3. Nalla S
    4. García-Martínez D
    5. Nalley TK
    6. Eyre J
    7. Prang TC
    8. Bastir M
    9. Schmid P
    10. Churchill SE
    11. Berger LR

    (2018) The vertebrae, ribs, and sternum of Australopithecus sediba

    PaleoAnthropology pp. 156–233.

    https://doi.org/10.4207/PA.2018.ART113

    • Google Scholar
74. 1. Wood B
    2. Constantino P

    (2007) Paranthropus boisei: fifty years of evidence and analysis

    American Journal of Physical Anthropology 134:106–132.

    https://doi.org/10.1002/ajpa.20732

    • Google Scholar
75. Book

    1. Wood B
    2. Schroer K

    (2017) Paranthropus: Where do things stand?

    In: Marom A, Hovers E, editors. Human Paleontology and Prehistory. Vertebrate Paleobiology and Paleoanthropology. Springer. pp. 95–107.

    https://doi.org/10.1007/978-3-319-46646-0

    • Google Scholar

Author details

1. Anjali M Prabhat

   Anthropology, Dartmouth College, Hanover, United States

   Contribution

   Conceptualization, Data curation, Formal analysis, Investigation, Methodology, Writing – original draft, Writing – review and editing

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0003-0654-3455

2. Catherine K Miller

   1. Anthropology, Dartmouth College, Hanover, United States
   2. Ecology, Evolution, Ecosystems, and Society, Dartmouth College, Hanover, United States

   Contribution

   Data curation, Formal analysis, Methodology, Writing – original draft

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-0352-3777

3. Thomas Cody Prang

   Department of Anthropology, Texas A&M University, College Station, United States

   Contribution

   Conceptualization, Data curation, Formal analysis, Methodology, Writing – review and editing

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0003-3032-8309

4. Jeffrey Spear

   1. Center for the Study of Human Origins, Department of Anthropology, New York University, New York, United States
   2. New York Consortium in Evolutionary Primatology, New York, United States

   Contribution

   Data curation, Formal analysis, Methodology, Writing – review and editing

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-0290-7090

5. Scott A Williams

   1. Center for the Study of Human Origins, Department of Anthropology, New York University, New York, United States
   2. New York Consortium in Evolutionary Primatology, New York, United States

   Contribution

   Conceptualization, Formal analysis, Methodology, Supervision, Writing – review and editing

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0001-7860-8962

6. Jeremy M DeSilva

   1. Anthropology, Dartmouth College, Hanover, United States
   2. Ecology, Evolution, Ecosystems, and Society, Dartmouth College, Hanover, United States

   Contribution

   Conceptualization, Formal analysis, Investigation, Methodology, Supervision, Writing – original draft, Writing – review and editing

   For correspondence

   Jeremy.M.DeSilva@dartmouth.edu

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0001-7010-1155

• 2,809

  views

• 237

  downloads

• 10

  citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.