sign in sign up
<<
Home , Bipedalism, Gait (human), Oreopithecus, Orthograde posture, Savannah hypothesis

with other , we use considerably less energy to move than do quadrupedal . While many have investigated the mechanics of JEREMY M. DESILVA and in , the extraordinary work of ELLISON J. MCNUTT Verne Inman (Saunders, Inman, and Eberhart Dartmouth College, USA 1953) was the first to detail the major deter- minants of bipedal efficiency in humans. Skeletal correlates of bipedal gait are listed below. sapiens is the only extant that habitually strides only on its extended —a type of locomotion referred to as bipedalism. Certainly there have been (e.g., Musculoskeletal theropod ) and there continue to be for bipedalism (e.g., ratite ) other striding bipeds. Addi- tionally, many mammals are habitually upright By comparison with the musculoskeletal system and use saltatory locomotion (e.g., kangaroos, of our closest relatives, the one has , springhares). Some even are facultative evolved (or, for some , ontogenetically bipeds: they stride, albeit infrequently, on two developed) characters functionally correlated feet during short bouts of locomotion. This has withouruniqueformoflocomotion.Many been observed in , some , and will be described below, but this should not be in modern . Humans are unique among regarded as a complete list. The human foramen mammals in being obligate bipeds. magnum is in an anterior position, which bal- While it remains unclear why bipedalism ances the head atop a nearly vertical spine. The evolved, this form of locomotion has two obvious spine itself is curved, with lordotic lumbar and advantages. First, it releases the upper from cervical regions and a kyphotic thoracic region. any locomotor responsibilities and thus provides The is greatly modified by comparison a form of transport consistent with the develop- with the ape pelvis. The ilia are short and stout, ment of and eventual reliance on tools. Darwin which lowers the center of mass by reducing (1871) (see darwin, charles r.) himself hypo- the distance between the sacroiliac joint and the thesized that the freeing of the for stone acetabulum. Furthermore, the iliac blades are tool construction was a critical selective pressure sagittally oriented, which repositions the lesser that drove bipedal locomotion. As the discov- gluteals (gluteus medius and gluteus minimus) ery and accurate dating of and artifacts andconvertsthemintoabductors.Thisreorien- necessary to test this hypothesis occurred first tation prevents pelvic tilt during single-legged in the 1960s and (e.g., 1.85 Ma Oldowan stance phase. Humans possess long , which tools; 3.66 Ma ), the antiquity of are functionally important for increasing stride bipedalism in relation to stone tool construction length. The weight-bearing joints of the lower appeared to refute Darwin’s hypothesis about the limb are enlarged and have a large volume of origins of upright walking. However, since the trabecular bone, which is able to dissipate the evidence for stone tool production and use was high forces incurred on an upright skeleton pushed back to ∼3.4 Ma and the oldest secure and to spare nonrenewable cartilage. The distal evidence for habitual bipedalism somewhere femur possesses a bicondylar, or carrying angle, between 3.66 Ma and 4.2 Ma, the temporal gap is which positions the knees and the feet directly closing and this hypothesis may deserve a second under the center of mass and reduces inefficient look. A second advantage of upright walking is mediolateral weight transfer during walking. This thatitisaremarkablyeconomicformoflocomo- is not present at birth; it develops in tod- tion. Although humans are slow by comparison dlers as they begin walking. Humans have a thick

The International Encyclopedia of Biological Anthropology.EditedbyWendaTrevathan. © 2018 John Wiley & Sons, Inc. Published 2018 by John Wiley & Sons, Inc. DOI: 10.1002/9781118584538.ieba0059 2 BIPEDALISM patella, which increases the moment arm (i.e., The proximal tibia possesses an expanded tibial length) for the quadriceps—a muscle important plateau, adaptive for dissipating high forces at forpreventingbucklingofthekneeduringthe thekneeduringbipedalgait.Furthermore,the single-legged stance phase and for extension distal tibial shaft is orthogonal to the plane of during the swing phase. The tibia is orthogonal in the joint, which would have positioned relation to the , which aligns the lower limbs the knee directly above the foot—an orientation andpositionsthefootinanevertedset. found in humans that functionally minimizes the Unsurprisingly, many adaptations to bipedal- costly displacement of the center of mass in the ismcanbefoundinthefoot,whichistheonlypart coronal plane and is correlated with a bicondylar of our body that is in contact with the substrate angle. This latter point is particularly important, during locomotion. The Achilles tendon is long given evidence that the bicondylar angle is devel- and the arch of the foot is well developed. These opmentally plastic and appears to occur only in soft-tissue adaptations are thought to increase the the context of extended knee bipedalism. elasticenergyreturnsoastoaidinpropulsion, Material assigned to ramidus particularlywhilerunning.Therelativeexpan- from the 4.4-million-year-old Aramis site in sion of the proximal calcaneus and the plantar the Middle Awash, Ethiopia has been proposed position of the lateral plantar process have been to come from a bipedal hominin. These claims proposed as adaptations that dissipate the large are based primarily on the morphology of the forces directed through the calcaneus during heel pelvis, femur, and partial foot (White et al. 2009). strike.Thegreattoeisadducted—fullyaligned The reconstructed pelvis possesses a human-like with the other digits. This orientation, together ilium and a more ape-like ischium. Most salient with the attachment of the plantar aponeurosis (a are the somewhat flaring, sagittally oriented thick band of tissue from the calcaneus ilia, which would allow the lesser gluteals to to the proximal phalanges), renders the foot stiff act as abductors during bipedal gait in Ardip- during heel lift and helps convert the foot into ithecus.Furthermore,theiliaappeartobewell a rigid propulsive lever. The tarsals are relatively spaced in the coronal plane, freeing the lumbar elongated,whilethephalangesarequiteshort. vertebrae to be lordotic during bipedal gait. Finally, the metatarsal heads are domed and However,thepelvisiscrushedandthisinter- the proximal phalanges canted—anatomies that pretation relies on a digital reconstruction of indicate dorsiflexion of the metatarsophalangeal the fragmented remains. Recovery of additional material or an independent assessment of this joints during the push-off phase of bipedal walk- pelvic reconstruction will help test the hypothesis ing. Thus the human skeleton (see skeletal proposed. While the medial column of the foot biology in anthropology) exhibits anatomies is ape-like in possessing a grasping, abducted that are likely to be under genetic control and are hallux, the lateral column is rigid and may have true adaptations for bipedalism (e.g., reorienta- facilitated a primitive form of bipedal locomo- tion of the ilia) and anatomies that only develop in tion. Ardipithecus (see ARDIPITHECUS)possesses the context of bipedalism (e.g., bicondylar angle). robust metatarsal bases, domed heads of the lateral metatarsals, and dorsally canted proxi- mal phalanges. However, the talus is ape-like in When did bipedalism evolve? possessing a high trochlea laterally, an anatomy that suggests that the foot of Ardipithecus was While the evidence for a striding bipedal gait in an inverted set and not in an everted posi- in hominins around 3.66 Ma is unequivocal, tion, as in the later .Giventhe determining how far back in time this loco- functional link between a valgus knee and a extends has been more difficult. In our varusankle,thisankleanatomyinArdipithecus opinion, the oldest convincing skeletal evidence would be consistent only with a weakly devel- for habitual bipedal gait in hominins can be oped bicondylar angle, and thus with infrequent found in the 4.2-million-year-old KNM-KP bipedalism. 29285 tibia assigned to Australopithecus anamen- Bipedal locomotion has also been proposed sis (see /australopith). for Ardipithecus kadabba on the basis of the BIPEDALISM 3 dorsal tilt of a pedal phalanx (AME-VP-1/71) confirmation of bipedal locomotion will neces- from 5.2-million-year-old sediments in the Mid- sitate the recovery or publication of postcranial dle Awash, Ethiopia (Haile-Selassie 2001). This elements. anatomy, canted to the proximal facet, suggests Some have proposed that the late dorsiflexion at the metatarsophalangeal joint and (∼8Ma)ItalianapeOreopithecus may have been a more human-like off mechanism. While the bipedalonthebasisofanatomiesofthepelvisand anatomyofthisfossilistantalizing,itisdifficult the foot (Köhler and Moyà-Solà 1997). Of course, to assess bipedalism in a species on the basis of bipedal locomotion in would be a single toe bone; further finds will be needed to fascinating and scientifically quite important test this hypothesis. precisely because this hominoid is unlikely to Three proximal femora, including a well- be an ancestor to hominins and would therefore preserved one (BAR 1002’00), have been recov- provide an example of parallelism. However, most ered from the 5.8–6.2-million-year-old Kenyan of the scientific community remains unconvinced that Oreopithecus was bipedal. tugenensis (see ORRORIN)and hypothesized to come from a bipedal hominin. In In sum, habitual bipedalism undoubtedly evolved about 4 Ma, but evaluating claims that fact, early observations suggested that the Orrorin this form of locomotion was an important part femur was more human-like than specimens of the locomotor repertoire of hominins earlier assigned to Australopithecus (Senut et al. 2001). in the , or even in the late Miocene, Continued work on this specimen finds either lit- will require additional fossil evidence. Further- tle difference between Orrorin and australopiths more, although bipedalism is often presented as or similarities between Orrorin and Miocene a defining feature of the hominin lineage, current hominoid femora. The Orrorin femur has a mod- evidence suggests that this form of locomotion erately elongated neck, a hominin feature that may have evolved well after the hominin split would increase the mechanical advantage of the with the lineage, given the paucity of fos- lesser gluteals during the single-legged stance silsfromthelateMioceneandestimatesthat phase of walking. However, the distribution of place the divergence data as far back as at least cortical bone around the femoral neck is not as 7–8 Ma. asymmetrical as anticipated in a biped and may be evidence of a different form of gait. Again, only additional fossils will help assess claims for From what did bipedalism evolve? bipedalism in Orrorin. tchadensis (see SAHELANTHRO- Just as uncertain as when bipedalism evolved PUS)isa∼7-million-year-old hominid from Chad, is the question of the body form from which Central Africa. There are no published postcra- bipedalism evolved. A handful of different mod- nialbonesfromthisMiocenetaxon;bipedalism els have been proposed to explain how this hasbeeninferredinsteadfromthepositionof locomotion could evolve from our ape ances- the on both the original skull try. Most researchers have recognized that the (Brunet et al. 2002) and its digital reconstruction. modern hominoids are all orthograde animals, The foramen magnum is anteriorly positioned capable of holding their bodies in an upright and forms an angle with the plane of the orbits posture—potentially preadapting our ancestors that is closer to the range of this angle in humans to bipedalism. Early scholars embraced a hylo- and australopiths than to the range in African batid model for the origins of bipedalism (e.g., great apes. However, this interpretation has been Keith 1923). will occasionally locomote contested on the basis of (1) the morphology on two legs and are highly upright in an arboreal of the nuchal plane and (2) uncertainty in the context. Keith (see keith, arthur) (1923), and relationship between the position of the foramen later on Morton (see morton, dudley j.) (1926), magnum and bipedal locomotion. The foramen hypothesizedthatanuprightformoflocomotion magnum’s position may indicate an upright, in an orthograde ape may have predisposed our in Sahelanthropus,but lineage to bipedalism. As it became clear that 4 BIPEDALISM humansaremostcloselyrelatedtotheAfrican Why did bipedalism evolve? great apes and to in particular, Washburn (see washburn, sherwood l.) (1967) Just as it is still unclear precisely when bipedalism hypothesized that humans developed bipedalism evolved and from what, why bipedal locomotion from a -like ancestor and that we was selectively advantageous in the hominin had passed through a knuckle-walking stage. lineageremainsamystery.Giventhecomplete This “ground-up” approach to bipedal origins, absence of another habitually bipedal mammal in which a knuckle walker evolves into a biped, to serve as an analogue, testing origin stories contrasts with a “top-down” approach, in which is difficult, if not impossible (Cartmill 1990). upright walking evolves from an already upright, Nevertheless, hypotheses as to why hominins vertically climbing, arboreal ape. Tuttle (1981) evolved bipedal locomotion abound (see Rose challenged the idea that bipedalism evolved from 1991 for a full treatment, with bibliography). As a knuckle-walking ancestor and instead pro- we have seen, Darwin (1871) and scholars after posed that an arboreal climber was a more likely him suggested that bipedal locomotion freed the predecessor. Most recently, Thorpe, Holder, and hands for tool use. Others distanced the carrying Crompton (2007) found evidence for frequent hypothesis from tools and instead invoked the bouts of -assisted bipedality in carryingofinfantsorofvaluablefooditems—as and proposed that upright walking may have is occasionally observed in chimpanzees. Food emerged from a highly arboreal, orthograde ani- gathering, specifically by females, was proposed mal that was bipedal in the trees. These models as a possible selective advantage for bipedalism for the origins of bipedalism are ape-based (either (Tanner and Zihlman 1976), as was the freeing generally, Morton 1926, or specifically, Washburn of the hands for picking seeds, as witnessed in 1967) and stem from the fact that humans are modern (Jolly 1970). Food carrying is orthograde hominoids. However, Straus (see also the foundation for Lovejoy’s (1981) provi- straus, william l.) (1949) recognized decades sioning model, which posits that a bipedal male ago that humans share many features with cerco- could carry more food to attract and provision a pithecoid monkeys. He interpreted these data to mate and that this would eventually lead to the mean that humans represent a deep - evolutionofanadaptivecomplexconsistingof ary lineage, separate from that of the apes. Yet bipedalism, canine reduction, concealed ovula- the same data could also mean that the human tion, and pair-bonding. Food gathering is also the form is more primitive and that the modern centerpiece of Kevin Hunt’s “low-hanging fruit” apes have become highly derived in the time hypothesis, which uses modern chimpanzee since the Miocene radiation of hominoids. Most behavior to argue that bipedalism evolved initially recently Lovejoy et al. (2009) have supported this as a postural for acquiring food. interpretation in their analysis of Ardipithecus. Whiletheuseofmodernchimpanzees While there is growing evidence that modern as a model for understanding the origins of apes have evolved considerably since the last bipedalism has been criticized, it remains com- common ancestor, it still remains unclear what monplace (see great apes as models for the body form of the last common ancestor may ). Bipedal locomotion occurs have been, and therefore from what locomo- in chimpanzees during aggressive display bouts tion bipedalism evolved. The paucity of fossils and may have been advantageous in hominins from the very period in which bipedalism was by freeing up their fists for fighting. There isa probably emerging (4–8 Ma) hampers efforts to less aggressive variant of the vigilance hypothesis testthehypothesespresentedabove.Further- (nicknamed the “peek-a-boo” hypothesis), in more, efforts to use modern as models which bipedalism evolved as a way for hominins for the origins of bipedalism are problematic if to safely scan the grassy savannah for predators. the body form from which bipedalism evolved An alternative but essentially untestable idea (the turned out to be a generalized ape with no extant “trenchcoat” hypothesis) proposes that bipedal- representation. ism evolved as a strategy for displaying one’s BIPEDALISM 5 genitalia. Assuming that the first bipeds occu- Bipedalism in Australopithecus pied an open (), some have argued that bipedalism reduces the Regardless of the selective reasons for bipedalism, surfaceareaofthebodyexposedtosunlightand this became the dominant (though probably therefore may have evolved as a thermoregula- not the only) form of locomotion in Pliocene tory adaptation (Wheeler, 1991). This view has australopiths. As discussed earlier, convincing been challenged by proponents of the thesis that evidence for habitual bipedalism can be found bipedalism first appeared in a wooded habitat in the 4.2-million-year-old Australopithecus ana- (White et al. 2009). Data showing that a bipedal mensis tibiacollectedbyateamledbyMeave gait is energetically efficient (Sockol, Raichlen, Leakey at Kanapoi, Kenya. Fossil footprints and Pontzer 2007) lend support to the notion that from Laetoli, Tanzania demonstrate that around this form of locomotion may have evolved in the 3.66 Ma a hominin was fully bipedal (Day and context of patchy resources and widely spaced Wickens 1980). The great toe is in line with the environments. Moving from one grove otherdigits,thereisanincipientarch,andthere of fruit trees to the next may have been energeti- is also evidence for a prominent human-like cally efficient on two legs rather than on four. One heel strike in a hominin who likely walked with final hypothesis (“the aquatic ape”) suggests that an extended hip and knee. However, others bipedalism evolved in hominins wading through have suggested that the great toe is more diver- shallow water. While this idea has been effectively gent than originally proposed (Bennett et al. dismantled, Richard Wrangham and a team of 2009). Furthermore, the G trackway was made colleagues have repurposed the hypothesis into by a hominin with an arch flatter than in most one of the “swamp ape,” in order to position humans today and with less medial weight trans- early bipedal hominins in a watery, sedge-rich fer to the great toe. Further experimental work habitat similar to today’s Okavango Delta in on formation, for example by Hatala, Botswana. suggests that the individual who produced the It seems at times that there are as many Gtrackwaywalkedwithamoreflexedposture hypotheses for why bipedalism evolved as there than humans do today. Therefore, although are researchers in our field. Why? Some of the Laetoli footprints are superficially quite thesehypothesesareuntestableandcannot human-like, they record subtle differences in be properly refuted and relegated to the dust- walking kinematics between the makers of the bin of science. Additionally, the absence of prints (presumably Australopithecus afarensis) another habitually bipedal mammal hampers and modern humans. our ability to use comparative methods to Considerable disagreement also surrounded test these hypotheses. It still remains unclear the functional analysis of the A. afarensis fossil exactly when we took our first steps and from material from 3.0–3.4 Ma deposits at Hadar, what body form this unusual form of locomo- Ethiopia, including the all-important skele- tion arose. The current absence of these data ton (Johanson et al. 1982). Work done primarily makesitdifficulttoplaceoriginhypothesesinto by C. Owen Lovejoy and Bruce Latimer (e.g., sharper focus. Assuming that the last common Latimer and Lovejoy 1989) interpreted the Hadar ancestor of humans and chimpanzees included lower limb and foot fossils as deriving from some bipedal posture and gait in its locomotor a hominin with a bipedal gait not unlike that repertoire, it remains possible that bipedalism found in humans today. The hip joint, while evolvedmorethanonce,andfordifferentrea- morphologically different from that found in sons. Furthermore, whether bipedalism evolved modern humans, would have been functionally once or multiple times, it is unlikely that there equivalent in preventing pelvic tilt during the was only one reason for it; hence many of the single-legged stance phase (Lovejoy, 1988). The above hypotheses—and likely some yet to be internal morphology of the femoral neck was conceived—may explain how and why bipedal- consistent with this human-like role of the lesser ism evolved, persisted, and flourished into the gluteals during bipedal walking. The morphology Pliocene. of the knee and ankle demonstrate a human-like 6 BIPEDALISM geometry of the lower limb and evidence for et al. 2016). These data point to a bipedal gait in a fully extended leg during walking. The large A. afarensis that would have been recognizably robust heel, the human-like great toe, and the more human-like than ape-like, but likely outside dorsally domed metatarsal heads combined with the range of modern human walking mechanics. dorsally canted phalanges were presented as However, new fossil discoveries from Ethiopia evidence for a foot with a human-like push-off have shown that Australopithecus afarensis was mechanism. These human-like, derived interpre- not the only biped at this time. Haile-Selassie tations of the Hadar fossils were systematically et al. (2012) described a 3.4 million-year-old foot published in response to initial interpretations of from Burtele that was morphologically more like the Hadar material as more ape-like in form and that of Ardipithecus than like that of A. afarensis. in inferred function. Stern and Susman (1983) TheBurtelefoothasnotfoundataxonomic identified more primitive anatomies in the Hadar home, though there is craniodental evidence for collection and interpreted them as evidence for another hominin—A. deyerimeda—in the area, a primitive bipedal gait, in which the hominins and for yet another— platyops—in walked with a bent hip and bent knee. Stern Kenyaatthistime.WhiletheBurtelefootpos- and Susman (1983) noted that the A. afarensis sessed domed lateral metatarsal heads and canted pelvis may have been more ventrally positioned, phalanges (consistent with a form of bipedalism), as in modern apes; the femoral head was small; the great toe was divergent and the metatarsal the legs were short; the knee, ankle, and great bases were weakly developed, as found in apes toe may have been more mobile; and the (specifically in modern ). Thus this impor- were longer and more curved. While many of tant fossil convincingly demonstrates diversity in these anatomies were consistent with arboreality, bipedal walking during the Pliocene. The South the researchers further argued that the Hadar African hominin “” (StW 573), which material was inconsistent with a human-like may represent Australopithecus prometheus,was bipedal gait in A. afarensis.TheStonyBrook originally proposed to also possess an abducent University interpretation of the Hadar material hallux (Clarke and Tobias 1995), but subsequent used the anatomy of the fossils to reconstruct analysis has revealed that the great toe is in the daily life of Australopithecus and provided line with the other digits. The ankle, however, strong evidence for an arboreal component to appears more primitive that that found in A. the locomotor repertoire of A. afarensis,which was practiced minimally to prevent predation afarensis (Harcourt-Smith and Aiello, 2004) and at night. However, Latimer (1991) and others “Little Foot” may very well provide additional have argued that climbing would have been evidence for bipedal variation in the Pliocene. adaptively insignificant, since the vector of evo- However, this hypothesis remains on hold until lutionary change was in a direction that led a full description of the StW 573 skeleton is away from arboreality. Ward (2002) summarized published. this argument clearly and explained how the Bipedal diversity likely continued into the seeming differences in the interpretation of the early as well. Primarily on the basis Hadar material are in part a result of researchers of pelvic and femoral remains from Sterkfontein asking different questions of the fossils (e.g., and Swartkrans, South Africa, Robinson (see daily life of Australopithecus versus anatomical robinson, john talbot) (1972) hypothesized targets of selection over time). Even granting that Australopithecus africanus and this, the two research groups proposed conflict- robustus locomoted in a different manner, the ing interpretations of how A. afarensis walked. former being more human-like. Harcourt-Smith More recent work on the postcranial skeleton and Aiello (2004) made a similar argument on (e.g., Haile-Selassie et al. 2010) would support the basis of differences in foot morphology in A. the interpretation that A. afarensis possessed a afarensis, A. africanus,andHomo habilis.These broadly human-like gait; however, there were authors proposed that A. afarensis possessed a likely subtle differences in hip and knee kine- human-like ankle in combination with a more matics, weight transfer across the foot, and the ape-like forefoot, while A. africanus had a more push-off mechanism in A. afarensis (Fernández human-like forefoot but a primitive tarsus. The BIPEDALISM 7 late South African australopith A. sediba also pos- skeletal morphology of late Pleistocene humans sesses a mosaic of foot morphology unlike that are consistent with modern human gait mechan- found in other Plio-Pleistocene hominins (Zipfel ics. However, changes in activity patterns related et al. 2011), which suggests a distinct, perhaps toamoresedentarylifestyleattheboundary autapomorphic, hyperpronatory form of bipedal between Pleistocene and Holocene has resulted locomotion (DeSilva et al. 2013). These varia- in a more delicate skeleton, which consists of less tions on an australopith Bauplan are likely due densetrabecularnetworksinourjoints(Chirchir to differences in local ecologies, substrates, and et al. 2015). degreesofrelianceonotherformsoflocomotion, such as climbing. While most regard the foot of the 1.85-million- Costs of bipedalism year-old OH 8 (Olduvai Hominid 8, accepted by many as H. habilis) as evidence for a human-like Bipedalism was obviously a selectively ben- form of bipedal locomotion (Day and Napier eficial form of locomotion for our ancestors 1964), there is some evidence that early Homo and extinct relatives—otherwise it would not was not fully modern in its locomotor mechanics have evolved. However, there is no such thing (Ruff 2009; Pontzer et al. 2010), and there is as an evolutionary “free lunch”, and there are growing evidence for locomotor diversity in our significant costs to bipedalism. Changes to the genusaswell.Thesedataderivefromanearly pelvis associated with the evolution of bipedalism Pleistocene Homo femur and pelvis from Kenya reduces the size of the birth canal and renders (Ward et al. 2015); unique anatomy in the South African hominin (Harcourt-Smith childbirth in humans more difficult than in apes et al. 2015); and anatomies of the late Pleistocene (e.g., Krogman 1951). While this “obstetrical island species (Jungers et al. dilemma” (Washburn 1960) predicts locomotor 2009) that would be consistent with a distinct costs to women who have not been supported by recent evidence (Warrener et al. 2015), high form of bipedal locomotion (see HOMO). General consensus has emerged that bipedal cephalopelvic ratios and therefore long, difficult locomotion kinematically indistinct from that labors may have existed since the Pliocene and found in modern humans first evolved in Homo are likely a consequence of bipedalism. erectus (or African ). This evidence There are also other costs to bipedalism. derives from footprint data (e.g., Bennett et al. Humans cannot gallop, and therefore our maxi- 2009) and from skeletal morphology primarily mum speed is quite slow by comparison with that discerned from a single, nearly complete juvenile of quadrupeds. Even the fastest human on earth skeleton from Nariokotome, Kenya (KNM-WT (Usain Bolt: 44.7 km/h) is considerably slower 15000). However, it must be noted that the than the African mammals our hominin ancestors postcranial anatomy of still differs mayhavewantedtocatch—thewildebeest—or from that of modern humans in subtle ways (e.g., to avoid—the lion (both clocked at ∼80.5 km/h, more flared ilia; platymeric femora; dorsoplan- almost twice the speed of the fastest human). By tarly squat talus). How these differences impacted evolving bipedalism, humans therefore sacrificed gait mechanics or energetic efficiency remains speed. Additionally, we sacrificed stability, given unknown. Furthermore, while the postcranial that with each stride we are positioned on a single anatomy of Middle Pleistocene hominins is support. predominantly human-like, subtle anatomical Bipedalism also causes musculoskeletal prob- differences have also been noted, for instance, in lems. Our vertical spine is subject to high the Sima de los Huesos hominins from Atapuerca, compressive forces that can exacerbate already in the 250,000-year-old Jinnuishan skeleton from uneven mediolateral loads during development China,andeveninNeanderthals.Thesedif- and may lead to —a condition not ferences are not generally attributed to unique uncommon in humans but exceptionally rare in gait mechanics but to more strenuous activity other mammals (Latimer 2005). Furthermore, the patterns, which often require more mediolateral has several curves in the sagittal motion on more varied substrates. Footprints and plane. In humans, compressive forces at the apex 8 BIPEDALISM ofthesecurvesresultinahighfrequencyof Clarke, R. J., and P. V. Tobias, P. V. 1995. “Sterkfontein compression fractures and, in the lumbar region, Member 2 Foot Bones of the Oldest South African in a high frequency of spondylolysis. Bipedal Hominid.” Science 269 (5223): 521–24. locomotion also takes its toll on the human foot, Darwin, C. 1871. The Descent of Man.London:Murray. Day, M. H., and J. R. Napier. 1964. “Hominid Fossils through injuries ranging from collapsed arches from Bed 1, Olduvai George, Tanganyika: Fossil Foot to ankle sprains (e.g., the anterior talofibular Bones.” 201: 969–70. ligament is the most frequently sprained liga- Day, M. H., and E. H. Wickens. 1980. “Laetoli Pliocene ment in the body). These injuries in humans are Hominid Footprints and Bipedalism.” Nature 286: notsolelytheresultofamodernlifestyle.Both 385–87. KSD-VP-1/1, a large male Australopithecus,and DeSilva,J.M.,K.G.Holt,S.E.Churchill,K.J. KNM-ER 2596, a small hominin from Koobi Carlson,C.S.Walker,B.Zipfel,andL.R.Berger. 2013. “The Lower Limb and Mechanics of Walking Fora, possess skeletal evidence for healed ankle in .” Science 340 (6129). fractures. OH 35 has a healed high-ankle sprain. doi:10.1126/science.1232999. OH 8 has osteoarthritis along the lateral forefoot Fernández,P.J.,N.B.Holowka,B.Demes,and and the cotylar fossa. Furthermore, Lucy pre- W. L. Jungers. 2016. “Form and Function of the serves evidence for a spinal pathology. Thus it Human and Chimpanzee Rearfoot: Implications for appears that the musculoskeletal costs of bipedal Early Hominin Bipedalism.” Scientific Reports 6. locomotion have been with us for some time. doi:10.1038/srep30532. Haile-Selassie, Y. 2001. “Late Miocene Hominids from Despite these costs, bipedalism was selectively theMiddleAwash,Ethiopia.”Nature 412 (6843): advantageous and became the dominant form of 178–81. locomotion for the hominin clade sometime after Haile-Selassie, Y., B. Latimer, M. Alene, A. Deino, L. its divergence from the panin lineage. Gibert,S.Melillo,B.Saylor,G.Scott,andC.Lovejoy. 2010. “An Early Australopithecus afarensis Postcra- SEE ALSO: /mechanobiology; nium from Woranso-Mille, Ethiopia.” Proceedings of East African fossil record; Functional the National Academy of Sciences 107 (27): 12121–26. morphology,postcranial,human;Hadar;Homo, Haile-Selassie,Y.,B.Saylor,A.Deino,N.Levin,M. Alene, and B. Latimer. 2012. A New Hominin early; Leakey, Mary; Malapa; Postcranial Foot from Ethiopia Shows Multiple Pliocene Bipedal morphology, nontraditional analysis; Schultz, Adaptations.” Nature 483 (7391): 565–69. Adolph H.; South African fossil record; Harcourt-Smith, W. E. H., and L. C. Aiello. 2004. ; Turkana Basin “Fossils, Feet, and the Evolution of Human Bipedal Locomotion.” Journal of Anatomy 204 (5): 403–16. Harcourt-Smith,W.E.H.,Z.Throckmorton,K.Con- gton, B. Zipfel, A. Deane, M. S. M. Drapeau, S. REFERENCES Churchill, L. Berger, and J. DeSilva. 2015. “The Foot of Homo naledi.” Nature Communications 6. Bennett,M.R.,J.W.Harris,B.G.Richmond,D. doi:10.1038/ ncomms9432. R. Braun, E. Mbua, P. Kiura, P. D. Olago, et al. Johanson,D.C.,C.Lovejoy,W.Kimbel,T.White, 2009. “Early Hominin Foot Morphology Based on S. Ward, M. Bush, B. Latimer, and Y. Coppens. 1.5 Million-Year-Old Footprints from , Kenya.” 1982. “Morphology of the Pliocene Partial Hominid Science 323 (5918): 1197–201. Skeleton (A. L. 288–1) from the Hadar Formation, Brunet, M., F. Guy, D. Pilbeam, H. T. Mackaye, A. Lik- Ethiopia.” American Journal of Physical Anthropology ius, A. D. Ahounta, A. Beauvilain, et al. 2002. “A New 57 (4): 403–51. Jolly, C. J. 1970. “The Seed-Eaters: A New Model of Hominid from the Upper Miocene of Chad, Central Hominid Differentiation Based on a Anal- Africa.” Nature 418 (6894): 145–51. ogy.” Man 5: 5–26. Cartmill, M. 1990. “Human Uniqueness and Theoretical Jungers,W.L.,W.E.H.Harcourt-Smith,R.E.Wunder- Content in .” International Jour- lich,M.W.Tocheri,S.G.Larson,T.Sutikna,R.A. nal of Primatology 11 (3): 173–92. Due, and M. J. Morwood. 2009. “The Foot of Homo Chirchir, H., T. L. Kivell, C. B. Ruff, J.-J. Hublin, floresiensis.” Nature 459 (7243): 81–84. K. J. Carlson, B. Zipfel, and B. G. Richmond. 2015. Keith, A. 1923. “Hunterian Lectures on Man’s Posture: “Recent Origin of Low Trabecular Bone Density Its Evolution and Disorders: Given at the Royal Col- in Modern Humans.” Proceedings of the National lege of Surgeons of England.” British Medical Journal Academy of Sciences 112 (2): 366–71. 1 (3251): 669–73. BIPEDALISM 9

Köhler, M., and S. Moyà-Solà. 1997. “Ape-Like or Rendus de l’Académie des Sciences, Series IIA: Earth Hominid-Like? The Positional Behavior of Oreo- and Planetary Science 332 (2): 137–44. pithecus bambolii Reconsidered.” Proceedings of the Sockol, M. D., D. A. Raichlen, and H. Pontzer. 2007. National Academy of Sciences 94 (21): 11747–50. “Chimpanzee Locomotor Energetics and the Origin Krogman, W. M. 1951. “The Scars of Human Evolu- of Human Bipedalism.” Proceedings of the National tion.” Scientific American 184: 54–57. Academy of Sciences 104 (30): 12265–69. Latimer, B. 1991. “Locomotor Adaptations in Australo- Stern, J. T., Jr., and R. L. Susman. 1983. “The Locomo- pithecus afarensis: The Issue of Arboreality.” In Orig- tor Anatomy of Australopithecus afarensis.” Ameri- ine(s)delabipédiechezlesHominidés,editedby can Journal of Physical Anthropology 60 (3): 279–317. Y. Coppens and B. Senut, 169–76. Paris: Centre Straus, W. L. 1949. “The Riddle of Man’s Ancestry.” National de la Recherche Scientifique. Quarterly Review of Biology 24 (3): 200–223. Latimer, B. 2005. “Editorial: The Perils of Being Tanner, N., and A. Zihlman. 1976. “Women in Evo- Bipedal.” Annals of Biomedical Engineering 33 (1): lution, Part I: Innovation and Selection in Human 3–6. Origins.” Signs 1 (3): 585–608. Latimer, B., and Lovejoy, C. O. 1989. “The Calcaneus of Thorpe,S.K.S.,R.L.Holder,andR.H.Crompton. Australopithecus afarensis and Its Implications for the 2007. “Origin of Human Bipedalism as an Adapta- Evolution of Bipedality.” American Journal of Physi- tion for Locomotion on Flexible Branches.” Science cal Anthropology 78 (3): 369–86. 316 (5829): 1328–31. Lovejoy, C. O. 1981. “The Origin of Man.” Science 211 Tuttle, R. H. 1981. “Evolution of Hominid Bipedalism (4480): 341–50. and Prehensile Capabilities.” Philosophical Transac- Lovejoy, C. O. 1988. “Evolution of Human Walking.” tions of the Royal Society of London B: Biological Scientific American 259 (5): 118–25. Sciences 292 (1057): 89–94. Lovejoy,C.O.,G.Suwa,S.Simpson,J.Matternes,and Ward, C. V. 2002. “Interpreting the Posture and Loco- T. White. 2009. “The Great Divides: Ardipithecus motion of Australopithecus afarensis:WhereDoWe ramidus Reveals the Postcrania of Our Last Common Stand?” American Journal of Physical Anthropology Ancestor with African Apes.” Science 326 (5949): 119 (S35), 185–215. 73–106. Ward,C.V.,C.Feibel,A.Hammond,L.Leakey,E.Mof- Morton, D. J. 1926. “Evolution of Man’s Erect Posture fett,J.Plavcan,M.Skinner,F.Spoor,andM.Leakey. (Preliminary Report).” Journal of Morphology 43 (1): 2015. “Associated Ilium and Femur from Koobi Fora, 147–79. Kenya, and Postcranial Diversity in Early Homo.” Pontzer, H., C. Rolian, G. Rightmire, T. Jashavili, M. Journal of Human Evolution 81: 48–67. PoncedeLeón,D.Lordkipanidze,andC.P.E. Warrener, A. G., K. L. Lewton, H. Pontzer, and D. E. Zollikofer. 2010. “Locomotor Anatomy and Biome- Lieberman. 2015. “A Wider Pelvis Does Not Increase chanics of the .” Journal of Locomotor Cost in Humans, with Implications for Human Evolution 58 (6): 492–504. the Evolution of Childbirth.” PLoS one 10 (3), Robinson, J. T. 1972. Early Hominid Posture and e0118903. Locomotion. Chicago, IL: University of Chicago Washburn, S. L. 1960. “Tools and Human Evolution.” Press. Scientific American 203: 63–75. Rose, M. D. 1991. “The Process of Bipedalization Washburn, S. L. 1967. “Behaviour and the Origin of in Hominids.” In Origine(s) de la bipédie chez les Man.” Proceedings of the Royal Anthropological Insti- Hominidés,editedbyY.CoppensandB.Senut, tute of Great Britain and Ireland 3: 21–27. 37–48. Paris: Centre National de la Recherche Scien- Wheeler, P. E. 1991. “The Thermoregulatory Advan- tifique. tages of Hominid Bipedalism in Open Equatorial Ruff, C. 2009. “Relative Limb Strength and Locomo- Environments: The Contribution of Increased Con- tion in .” American Journal of Physical vective Heat Loss and Cutaneous Evaporative Cool- Anthropology 138 (1): 90–100. ing.” Journal of Human Evolution 21 (2): 107–15. Saunders, J. B., V. T. Inman, and H. D. Eberhart. 1953. White,T.D.,B.Asfaw,Y.Beyene,Y.Haile-Selassie, “The Major Determinants in Normal and Patholog- C. Lovejoy, G. Suwa, and G. WoldeGabriel. 2009. ical Gait.” Journal of Bone and Joint Surgery 35 (3): “Ardipithecus ramidus and the Paleobiology of Early 543–58. Hominids.” Science 326 (5949): 64–86. Senut,B.,M.Pickford,D.Gommery,P.Mein,K. Zipfel, B., J. DeSilva, R. Kidd, K. Carlson, S. Churchill, Cheboi, and Y. Coppens. 2001. “First Hominid from and L. Berger. 2011. “The Foot and Ankle of Australo- the Miocene (Lukeino Formation, Kenya).” Comptes pithecus sediba.” Science 333 (6048): 1417–20.