Anthropological Science Review Vol. 127(1), 1–12, 2019

How did humans acquire erect bipedal walking?

Tasuku Kimura1* 1The University Museum, The University of Tokyo, Tokyo, Japan

Received 25 September 2018; accepted 19 February 2019

Abstract Recent fossil records have suggested that human erect bipedal locomotion started in Africa probably more than 6 million years ago. However, debate continues regarding how locomotion was ac- quired by our prehuman ancestors. Fossils and the genetic traits of recent humans and animals cannot answer this question directly. Therefore, the present paper reviews acquisition models of human biped- alism and explanations regarding how humans acquired bipedalism based on a comparative kinesiology of contemporary mammal species. Nonhuman primates are adequate models of human bipedal acquisi- tion because of not only the phylogenetically close relationship with humans, but also the trend toward hindlimb dominance and orthograde positional behavior in daily life. Although dissimilar to the erect bipedalism seen in humans, nonhuman primates adopt bipedal positional behavior in the wild. All non- human primates use the arboreal environment, but some groups of species utilize the ground predomi- nantly. Compared with relatively terrestrial nonhuman primates, relatively arboreal primates show more similarities with humans in their bipedal locomotion. Comparisons among primate species and between nonhuman primates and nonprimate mammals indicate that human-like bipedal characteristics are strongly related to arboreal life. Our prehuman ancestors likely started and adapted to bipedal locomo- tion while living in trees; this process is referred to as the generalized arboreal activity model. When humans began terrestrial locomotion, they likely performed proficient bipedalism from the first step. The generalized arboreal activity model presented here does not contradict the fossil records.

Key words: primates, bipedalism, orthograde, hindlimb dominance, arboreal activity

lion years ago (Ma) (Lovejoy et al., 2009a), and possibly Introduction more than 6 Ma (Senut et al., 2001; Brunet et al., 2002). On Human locomotion is characterized by bipedalism with the other hand, other specialties of present humans, such as an orthograde trunk on extended lower limbs. The trunk and large brains and developed tools, developed relatively more spine stand vertically and the hip and knee joints extend recently. The oldest stone tools discovered appeared around greatly. Although many vertebrates, including birds, kanga- 3 Ma (Harmand et al., 2015), and large brains similar to ours roos, and some lizards and dinosaurs, have walked or contin- were acquired only a few hundreds of thousand years ago ue to walk bipedally, this is usually done with pronograde (Henneberg and de Miguel, 2004). Erect bipedal locomotion trunk orientation and flexed hip joints, similar to quadru- is the oldest characteristic to distinguish humans from other peds. No extant or extinct vertebrates on earth other than vertebrates. The acquisition of erect bipedalism is the key to humans have acquired habitually erect bipedalism. Erect bi- defining hominoid fossils as human ancestors. pedalism is the one of the most specialized characteristics of When, where, how, and why did our human ancestors ac- humans. Because of the acquisition of bipedalism, human quire bipedal locomotion? In the last few decades, many at- hands became free from locomotion and able to be used for tempts have been made to answer these questions. The old- manipulating and carrying tools, food, and infants, even est human fossils were discovered from strata of between 4 during locomotion. It has been suggested that the large brain and 7 Ma in Africa, as described above. The phylogenetical- and vocal language of present humans were related to the ly nearest extant animals of human lineage, i.e. African great erect bipedalism (Schultz, 1942; Clark and Henneberg, apes, live in Africa. Human ancestors should have started 2017; Xu et al., 2018). When looking at human lineage bipedal locomotion in Africa around this time or a little ear- through the fossil record, bipedalism started at least 4.4 mil- lier. Many models have suggested how erect bipedalism may have begun. Fossils are useful for indicating the time and place of evolutionary processes, but locomotion traits should * Correspondence to: Tasuku Kimura, The University Museum, The University of Tokyo, Hongo 7-3-1, Bunkyo-ku, Tokyo 181-0033, be compared and discussed based on living animals because Japan. fossils cannot walk themselves. Explanation of fossil loco- E-mail: [email protected] motion can be sought only from extant animals. Compara- Published online 2 April 2019 tive kinesiology of living nonhuman primates is an impor- in J-STAGE (www.jstage.jst.go.jp) DOI: 10.1537/ase.190219 tant method of analysis to clarify the process of human

© 2019 The Anthropological Society of Nippon 1 2 T. KIMURA Anthropological Science bipedal acquisition (Kimura et al., 1979; Schmitt, 2003). mammals, except the woolly opossum, which is an arboreal Nonhuman primates frequently stand and walk bipedally, marsupial (Schmitt and Lemelin, 2002), usually exhibit larg- and are therefore useful animal models to study human bi- er vertical and backward force components in the forelimbs pedalism, not only because of their phylogenetically close than in the hindlimbs during quadrupedal walking (Manter, relationship with humans, but also because of their easy and 1938; Barclay, 1953; Björck, 1958; Pratt and O’Connor, customary bipedalism ability. A comparison between biped- 1976; Kimura et al., 1979). al walking in humans and nonhuman primates may clarify Among the nonhuman primates, monkeys that habitually the unique characteristics of human bipedalism. Because walk on the ground, such as baboons, Japanese macaques, locomotion of fossils might not be the same as that of living rhesus macaques, and patas monkeys, do not always exhibit animals, a simple comparison with one or two living species clear hindlimb dominance in terms of foot force. In these is not adequate to clarify the problem. Therefore, the present animals, the hindlimb force is sometimes equal to or less article reviews the models and empirical evidence on the than the forelimb force. On the other hand, arboreal primates process of human bipedal acquisition based on comparative that mainly utilize the arboreal environment, such as chim- kinesiology among multiple primate species and between panzees, orangutans, spider monkeys, and capuchins, typi- nonhuman primates and nonprimate mammals to present a cally show clear hindlimb dominance in terms of foot force generalized arboreal activity model. (Kimura et al., 1979; Kimura, 1992; Demes et al., 1994; Schmitt and Hanna, 2004). This suggests that hindlimb dom- Unique positional behavior of nonhuman primates inant force distribution is associated with arboreal life. The footfall order of common mammals during symmetri- Compared with nonprimate terrestrial mammals, which cal quadrupedal walking is usually the sequence RH-RF- are referred to in the present article as ‘common mammals,’ LH-LF (Howell, 1944; Hildebrand, 1967; Cartmill et al., nonhuman primates have several unique characteristics in 2002), where R is right, L is left, F is forelimb, and H is terms of their positional behavior. hindlimb; this is referred to as the lateral sequence Measurements of body weight distribution of the fore- (Hildebrand, 1967) or the backward cross type (Iwamoto and hindlimbs while in the quadrupedal standing position and Tomita, 1966). By contrast, nonhuman adult primates show that in common mammals, the forelimbs are usually usually adopt the sequence RH-LF-LH-RF (Prost, 1965; dominant, about 60% of body weight (Thompson, 1917; Tomita, 1967; Hildebrand, 1967; Rollinson and Martin, Iwamoto and Tomita, 1966). By contrast, the hindlimbs are 1981), which is referred to as the diagonal sequence or the usually dominant in nonhuman primates (Krüger, 1943; forward cross type (Figure 1). In both arboreal and terrestrial Iwamoto and Tomita, 1966; Kimura et al., 1979). During environments, forelimbs steer the body during quadrupedal quadrupedal locomotion, including asymmetrical high- locomotion. During the diagonal sequence, the hindlimb speed locomotion, in nonhuman adult primates, the hind- touches down on the substrate at about the same point as that limbs mostly put larger foot force components in the verti- of the forelimb on the same side and nearly under the body’s cal, i.e. body supporting, and backward, i.e. accelerating, center of the gravity. When the substrate contains large gaps directions compared with the forelimbs (Kimura et al., 1979; or consists of mechanically weak twigs, which are common Kimura, 1985, 1992, 2000; Reynolds, 1985; Demes et al., traits of the arboreal environment, the diagonal sequence is 1994; Schmitt and Hanna, 2004). By contrast, adult common convenient for the hindlimbs, which mainly support the

Figure 1. Quadrupedal and bipedal walking. From left to right, a quadrupedal dog representing the common mammal, the quadrupedal and bi- pedal walking of a chimpanzee, and a bipedal human, respectively. Black circles indicate the center of gravity of the body, which is higher in the bipedal than in the quadrupedal position. The quadrupedal footfall order of nonhuman primates is mainly a diagonal-sequence in which the fore- and hindfoot of the same side touch the substrate at about the same place at successive times. Common mammals mainly adopt the lateral-sequence, where the fore- and hindfoot of the same side touch at quite separate places. Many common mammals touch the substrate mainly with their toes and interdigital pads (digitigrade), but many arboreal nonhuman primates such as chimpanzees support their body with their whole sole (plantigrade), similar to humans. In nonhuman primates, the distal humerus is positioned in front of the shoulder at forefoot touchdown during quadrupedal walk- ing. On the other hand, the excursion of the humerus is not so large in common mammals. Vol. 127, 2019 HOW DID HUMANS ACQUIRE ERECT BIPEDAL WALKING? 3

Figure 2. Functional differentiation of the limbs in quadrupedal nonhuman primates. Nonhuman primates show larger acceleration and body supporting force components in the hindlimbs than in the forelimbs during quadrupedal locomotion. By contrast, common mammals accelerate and support the body mainly using the forelimbs. The steering activity of both groups is situated at the front. Nonhuman primates utilize mainly front-steering/rear-driving locomotion, whereas common mammals utilize mainly front-steering/front-driving locomotion (Kimura et al., 1979). body in nonhuman primates, compared with the forelimbs, behavior, constituting over 61% of the total observations in which touch down on the substrate and support the body at a chimpanzees. Sitting and squatting are the most common point relevant to where the forelimb on the same side has postural behaviors in trees for wild adult western lowland already been supported (Cartmill et al., 2002). Kinkajous gorillas, although there are significant seasonal and sex dif- and opossums, which are nonprimate arboreal mammals, ferences (Remis, 1995). Nonhuman primates often sit while also show a diagonal footfall sequence (Hildebrand, 1967; supporting their upper body with their hindlimbs and/or Cartmill et al., 2002). The main driving and supporting func- haunches and their forelimbs free. The functional differenti- tions of nonhuman primates are borne by the hindlimbs, as ation between the fore- and hindlimbs is clear in the sitting described above. Nonhuman primates exhibit functional position. The muscles, internal organs, and circulatory or- differentiation between the fore- and hindlimbs during quad- gans of the upper body should be accustomed to the or- rupedal locomotion, namely front-steering/rear-driving lo- thograde position (Keith, 1923). Nonhuman primates can comotion, in contrast to the front-steering/front-driving lo- easily stand bipedally from their orthograde sitting posture comotion of common mammals (Kimura et al., 1979) by utilizing their relatively strong hindlimbs. (Figure 2). Extant nonhuman primates have larger limbs than com- Primate quadrupedal locomotion is unique in comparison mon mammals. The limb bones, especially the hindlimb with that of common mammals, showing a more protracted bones, of primates are relatively longer (Alexander et al., arm and forelimb at the forefoot touchdown of a step 1979), larger in diameter, and more robust than those of (Larson et al., 2000). The distal humerus is positioned in common mammals based on a comparison of body mass front of the shoulder joint (Figure 1). The total excursion control (Kimura, 1991, 1995; see also Polk et al., 2000) (Fig- angles of both the humerus and forelimb of nonhuman pri- ure 3). The bones of some arboreal mammals, such as kinka- mates are larger than those of common mammals, except for jous, sloths, and possums, are also large (Kimura, 1995). two arboreal species, the woolly opossum and the koala. Interestingly, terrestrial humans share the same characteris- Larson et al. (2000) discussed the uniqueness of this charac- tics with other primates. On the other hand, many nonhuman teristic in relation to safe locomotion on and the grasping of primates that utilize the ground daily, such as patas mon- small branches. They noted that increased humeral excur- keys, baboons, and Japanese macaques, share some resem- sion mobility could be accomplished at the expense of joint blance with common mammals. The unique hindlimb domi- stability, which may be linked to the relatively small produc- nant positional behavior and long and robust limbs of tion force by the forelimbs compared with that of the hind- nonhuman primates can be explained by their adaptation to limbs. Larson et al. (2001) demonstrated that the thigh and the irregularly discontinuous arboreal space. In such three- hindlimb excursions were also larger in primate species than dimensional environments, animals travel up and down in common mammals. They claimed that large limb excur- while maintaining control of gravitational forces. Larger sion could be linked to the ability to increase speed without nonhuman primates usually move vertically with an or- increasing the step frequency, as well as to greater stability thograde trunk and upwardly oriented head, where gravita- and security on narrow substrates. tional forces are mainly supported by the hindlimbs. In the Nonhuman primates frequently sit with an orthograde arboreal environment, nonhuman primates use their long trunk and use the forefoot as a manipulating hand during forelimbs to forage for foods that are typically found on thin, foraging (Jolly, 1970), social communication, object play, flexible branches. In such situations, the hindlimbs should and even tool use. Kawai and Mito (1973) reported that the support the body on a thicker branch. Long and robust limb orthograde posture was assumed for 84% of the day by the bones and large shoulder excursion angles make it possible Formosan macaque; Morbeck (1975) showed that the to reach the food and pass safely over gaps. guereza’s sitting posture accounts for more than 50% of the Based on foot force patterns and bone robustness among total observations; and Hunt (1992) reported that excluding nonhuman primates, arboreal species are more hindlimb lying in a night nest, sitting was the most common positional dominant than terrestrial ones (Kimura et al., 1979; Kimura, 4 T. KIMURA Anthropological Science

Figure 3. Scatter diagram of osteological data for mammal limb long bones. The scatter diagram is based on principal component (PC) analysis from 25 linear measurements, the original data of which were divided by the cube root of body mass to eliminate differences in body mass. The first and second axes explain 65% of the variance. PC1 is the primary component associated with the large size, evenly controlled differences in body mass, especially epiphyseal diameters. Species on the positive side of PC2 have long metapodials and several forelimb bones with large diameters, whereas those on the negative side have long limb bones and several hindlimb bones with large diameters. Solid circles: 79 species of nonprimate quadrupedal mammals; open circles: 68 species of nonhuman primates, which form a clear group separate from the nonprimate mammals and are characterized by long bone lengths, except metapodials, and large bone diameters, especially of the hindlimbs; triangle: humans, which are in the nonhuman primate group. Additional letters: BV, brown-throated three-toed sloth; CC, golden-backed squirrel; CN, prehensile-tailed porcupine; PF, kinkajou; TG, common tupai; and TV, common brushtail possum from nonprimate mammals, all of which are active in arboreal environments and situated either among the primates or near the border of the two groups. In addition: EP, patas monkey; MF, Japanese macaque; PA, Anubis baboon; PH, hamadryas baboon from nonhuman primates, all of which use terrestrial surfaces daily and are located at the border of the two groups (Kimura, 1995).

2003), and arboreal non-primate species share a number of uated just above the hip joint near the vertebral column similar bone and locomotion patterns with nonhuman pri- while in the bipedal standing position. In nonhuman pri- mates (Kimura, 1985, 2002). These findings reinforce the mates, the center of gravity is situated ventral to the verte- arboreal influence on the positional characteristics of nonhu- bral column at the middle of the belly (Figure 1) (Kimura, man primates. 1996). The hip joint in nonhuman primates always flexes Primates who adapt to relatively arboreal environments during bipedal locomotion, never reaching human-like true show strong hindlimb dominance in their quadrupedal pos- hyperextension in which the thigh extends behind the trunk ture and locomotion, whereas relatively terrestrial nonhu- axis (Ishida et al., 1975; Yamazaki et al., 1983; Okada and man primates show weak hindlimb dominance. Arboreal Kimura, 1985; Okada et al., 1996). The knee joint in nonhu- species show large vertical and accelerating foot forces in man primates does not fully extend during the stance-phase. the hindlimbs and robust hindlimb bones. The hindlimb To fasten the flexed hip and knee joints against forces such dominance of primates, which is useful for bipedal walking, as body weight, both the flexor and extensor muscles work is likely acquired in the arboreal environment. simultaneously during the large part of stance-phase of walking (Ishida et al., 1975; Stern and Susman, 1981; Bipedal walking in nonhuman primates Vangor and Wells, 1983). In humans, the lower limb muscles work alternately and take long resting durations. Since hu- Many nonhuman primates include bipedal locomotion in man hip and knee joints extend in the middle of the stance- their daily locomotor repertories, in spite of having a high phase, i.e. in the single stance-phase, the center of gravity center of gravity and the difficulties involved in maintaining moves higher, increasing the body’s potential energy balance while in the bipedal compared with the quadrupedal (Kimura, 1996). Cavagna et al. (1976) and Alexander and position (Figure 1). Jayes (1978) showed that the high potential energy generat- The bipedalism of nonhuman primates, however, contains ed in each single stance-phase compensated for the loss of many characteristics that differ from that of humans. The forward kinetic energy. Part of the kinetic energy that was trunk of bipedal nonhuman primates never stands erect like input during the double stance-phase is recovered by the that of humans, but rather inclines forward (Figure 4). From transformation into gravitational potential energy in the sin- the side view, the center of gravity in the human body is sit- gle stance-phase. Thus, the human type of movement of the Vol. 127, 2019 HOW DID HUMANS ACQUIRE ERECT BIPEDAL WALKING? 5

Figure 4. Stick pictures depicting bipedal walking in a chimpanzee (left) and a human (right) on the sagittal plane. One cycle of walking from a heel-strike to the next heel-strike is shown. The statures of both species are depicted as equal in size. Sticks connect the tragion (ear point), shoul- der joint, hip joint, knee joint, ankle joint, and tip of the third toe in the chimpanzee, and the vertex, shoulder joint, hip joint, knee joint, ankle joint, and dorsal surface of the big toe in the human. Points on the head and toe are different in the two species because of the relatively differently shaped body parts. Human walking is characterized by an erect trunk with small angular movements, hyperextended hip joint, fully extended knee during the single stance-phase, and the rocking mechanism of the sole.

Figure 5. Correlation and regression analyses between the knee flexion angle and relative hip height during the stance-phase in chimpanzee bipedal walking. In total, 150 trials of chimpanzee bipedal walking from one year of age to adulthood were analyzed. The relative hip joint height is the highest hip height divided by the sum of the thigh and shank lengths. The knee flexion angle (degree) is obtained at the maximum extension, where 180° means full extension and smaller angles mean larger flexion. The correlation coefficient (0.427) is significant. The less flexed the knee during the stance-phase, the higher the height of the hip joint.

center of gravity economizes energy expenditures. Cavagna macaques, then recovery is small or nearly null. The vertical et al. (1976) calculated the ‘recovery’ of this mechanical foot force component in human walking, as measured by a energy during walking. In chimpanzees, this recovery is force plate, contains two peaks and a trough, at which time sometimes large, but other times small (Kimura, 1996). Af- the center of gravity moves higher during the single stance- ter touchdown, the flexed knee joint of nonhuman primates phase. By contrast, the vertical component in Japanese ma- flexes much more and the center of gravity moves lower. In caques and many nonhuman primates has only one peak in chimpanzees during walking, the maximum flexion of the which the center of gravity moves lower and the potential knee during the stance-phase correlates with the height of energy decreases (Kimura, 1985). Chimpanzees, orangu- the hip joint nearby which the center of gravity is situated tans, and spider monkeys, which are relatively arboreal spe- (Figure 5). When the knee joint stops flexion during the cies, sometimes walk with two peaks and a small trough, and single stance-phase, the center of gravity is kept relatively sometimes with a scarce trough (Kimura, 1985, 1996; high and recovery becomes large. When the knee joint is Pontzer et al., 2014). These animals walk in association with flexed substantially more during the entire single stance- large and sometimes with small recovery. Such irregulari- phase, as in the case of bipedal walking in most Japanese ties, individual and intraspecific, are one of the main charac- 6 T. KIMURA Anthropological Science teristics of bipedal walking in nonhuman primates, and are different costs within primate species could be related to the in striking contrast to the rhythmic, regular, and constant daily use of different environments. For arboreal nonhuman nature of human walking (Kimura and Yaguramaki, 2009). primates, the adoption of bipedal walking would have had O’Neill et al. (2015) pointed out that the large intraspecific only a small effect on walking costs; however, for relatively variance in kinematics would have been important raw ma- terrestrial monkeys, the energy cost of bipedal walking terial for natural selection. would have been high. The bipedal walking practiced among some but not all species of nonhuman primates is relatively similar to that in Models of human bipedal acquisition humans (Kimura et al., 1979). Hamadryas baboons and Jap- anese macaques walk with strongly flexed hip and knee Many models on the process of acquiring human bipedal- joints, and their energy recovery is low. Their heels do not ism have been presented. usually touch the substrate (digitigrade), similar to their 1. The terrestrial model quadrupedal walking (as in Schmitt and Larson, 1995; for an Terrestrial locomotion is thought to be a unique human exceptional case involving anubis baboons, see Berillon et characteristic in comparison with many monkeys and apes al., 2010). These species adapt to the relatively terrestrial that live mostly in arboreal environments. The bipedalism of environments of their daily lives. Spider monkeys and chim- our human ancestors has been discussed in regard to their panzees walk with relatively extended lower limb joints, al- debouch into the grassy plains (Senut et al., 2018). Some though not fully extended compared with humans. They primates frequently stand bipedally on the ground to look far usually touch the substrate with their entire soles (planti- into the distance or to collect food from the branches of grade), probably because they use relatively arboreal envi- small trees (Rose, 1976; Hunt, 1994). However, terrestrial ronments where they frequently grasp branches with their nonhuman primates cannot extend their hindlimb joints to a entire volar surfaces. Their calf muscles work strongly at the large extent because they are limited by the shortness of their take-off phase of walking, somewhat similar to humans muscles, ligaments, and the skin over their joints (Okada and (Ishida et al., 1975). Chimpanzees walk with a heel-strike on Kimura, 1985; Okada et al., 1996). Strong joint extension is the substrate and with a toe-off with their smaller toes (Fig- not necessary during quadrupedal locomotion, but is impor- ure 4). They can use the plantigrade rocking mechanism of tant for efficient bipedal locomotion. Among extant nonhu- the foot, similar to human walking, despite the differences in man primates, bipedal walking in the terrestrial ones differs the structure of the foot between chimpanzees and humans; substantially from that of humans in many regards, such as for example, their abducted big toe and lack of a sagittal arch flexed lower-limb joints, digitigrade touchdown, and weak (Holowka et al., 2017). The rocking mechanism of the foot hindlimb dominance, as previously described. Human bi- during double stance-phase is thought to help a conversion pedal acquisition is therefore difficult to establish from ter- of downward kinetic energy directly into forward kinetic restrial quadrupedalism. energy and to prolong step length (Cavagna et al., 1977). 2. The knuckle-walking model Spider monkeys have more flexible feet than chimpanzees, The phylogenetically closest living species to humans are and make touchdown from the lateral forefoot, but attain a African apes, i.e. common chimpanzees, bonobos, and goril- suitable posture for grasping by the entire sole (Okada, las. When these animals walk quadrupedally, they touch the 1985). dorsal side of their flexed fingers on the substrate. This loco- Twisting of the trunk, in which the shoulder and pelvis motion is referred to as knuckle-walking. Because their rotate opposite from each other, is a characteristic of walk- forelimbs are longer than their hindlimbs, their shoulders are ing in human adults and reduces angular momentum in the usually higher than their hips during quadrupedal standing. trunk. Nonhuman primates have some difficulty twisting the The knuckle-walking model supposes easy bipedal standing trunk in the same manner (Bramble and Lieberman, 2004; from such apes as a type of positional behavior (Morton, see also Thompson et al., 2015); their whole trunk rotates 1922). Quadrupedally walking chimpanzees, however, flex with the lower limb of the leading side when the step length their elbows during the stance-phase, and their shoulders are is long, regardless of whether the trunk twist is large or not always higher than their hips. In the hominoid lineage, small. gorillas are thought to have branched off before the diver- The metabolic cost of transport for chimpanzees is greater gence of humans and chimpanzees/bonobos. It seems more than that for common terrestrial mammals and birds when parsimonious to assume that knuckle-walking was acquired comparing the same body mass, whereas that for human by the common ancestors of humans and African apes, after walking is less costly (Sockol et al., 2007). Among chimpan- which it was lost by humans after diverging from the chim- zees, bipedal walking is not significantly more costly than panzee/bonobo lineage, than to assume that it developed in- quadrupedal walking (Taylor and Rowntree, 1973; Sockol et dependently and in parallel in the gorilla and chimpanzee/ al., 2007; Pontzer et al., 2014). No measurable difference is bonobo lineages after humans diverged from apes. Richmond apparent in the cost of walking on two or four legs for the and Strait (2000) proposed that knuckle-walking traits were capuchin monkey (Taylor and Rowntree, 1973). On the oth- apparent in the fossils of early hominids, but their evidence er hand, in Japanese macaques, the energy expenditure of was disputed and not widely accepted (Crompton et al., bipedal walking is higher than that of quadrupedal walking 2008; White et al., 2015; Senut et al., 2018). The knuckle- (Nakatsukasa et al., 2004, 2006). Chimpanzees and capu- walking of the African apes may have developed inde- chins are relatively arboreal primates, whereas Japanese pendently in parallel after diverging from the human lineage macaques use the terrestrial environment in daily life. The (Dainton and Macho, 1999; Kivell and Schmitt, 2009). Lo- Vol. 127, 2019 HOW DID HUMANS ACQUIRE ERECT BIPEDAL WALKING? 7 comotion may have been involved because of the adapta- 1993b), and about 10–18% in wild adult orangutans tions in hand structure in response to suspensory positional (Sugardjito and van Hooff, 1986; Cant, 1987). Vertical behavior (Tuttle, 1969). Suspensory adapted forelimbs and climbing could be one of the important preadaptations of the short hindlimbs of extant apes differ much from human bipedalism, but it is difficult to accept that vertical climbing limbs in which hindlimbs are much longer than forelimbs alone led to the acquisition of bipedal locomotion. (Erikson, 1963). 5. The generalized arboreal activity model 3. The brachiation model Based on comparative kinesiology among extant nonhu- Brachiation is suspensory locomotion that occurs while man primates, arboreal species such as chimpanzees, orang­ hanging onto branches with the forelimbs. Gibbons move utans, and spider monkeys show larger functional differen­ frequently by suspensory arm-swinging, including ricochet. tiation between the fore- and hindlimbs during quadrupedal The brachiation model has also been referred to as the ‘hylo- locomotion and greater resemblance to humans in bipedal batian model’ (Keith, 1923). Suspensory locomotion with- walking compared with relatively terrestrial species. This out ricochet was also acquired by the great apes. During resemblance may suggest the pathway via which our prehu- brachiation, the trunk orients vertically. The chests of gib- man ancestors acquired bipedalism, i.e. preadaptation to ar- bons are broader transversely than anteroposteriorly, similar boreal environments (Stern, 1975; Kimura et al., 1979; to those of humans, but dissimilar to those of common pron- Crompton et al., 2003, 2008; Thorpe et al., 2014; Senut et ograde mammals, where the dorsoventral diameter is large. al., 2018). Although both brachiators and vertical climbers Gibbons walk bipedally on level ground or on boughs. In adapted to arboreal locomotion, it remains difficult to devel- bipedal gibbons, the hip and knee joints are extended rela- op bipedal models only from each locomotion pattern, as tively widely during the stance-phase compared with other described above. Stern (1975) proposed that our arboreal nonhuman primates (Ishida et al., 1984). Due to the unique ancestors may have employed locomotion similarly to howl- bipedal walking of gibbons, the brachiation model has been er monkeys and orangutans, both of which are arboreal acti- proposed to account for pre-habitual bipedal walking vators. Orangutans mainly use arboreal environments with (Yamazaki et al., 1983). many kinds of positional behaviors. They are able to support Smooth brachiation with ricochet is difficult for large- their large bodies even with thin lianas with both pronograde bodied animals (Tuttle, 1975). Only infant chimpanzees, but and orthograde postures (Cant, 1987; Thorpe et al., 2009; not adults, spend long periods in orthograde suspensory Myatt and Thorpe, 2011). Howler monkeys show particular mode (Sarringhaus et al., 2014). The suspensory forelimbs similarities with humans in their hip and thigh musculature of gibbons are very long, and the body size and proportions (Stern, 1975). Extant nonhuman primates, however, are not of these primates are quite different from those in humans, human ancestors and evolved separately for each lineage who have long hindlimbs, relatively short forelimbs, and a after diverging from the human lineage (Senut et al., 2018). relatively large body size. The bipedal walking of gibbons For instance, the forelimbs are very long compared with the on flat substrates probably resulted from their difficulties in hindlimbs in all apes, in contrast to the relatively long hu- walking quadrupedally owing to their overly long forelimbs man hindlimbs. The differences in limb length are not large compared with their hindlimbs. It is difficult to link brachia- in howler and spider monkeys (Erikson, 1963), like other tion with the development of strong hindlimbs, which are generalized quadrupedal monkeys, but these species have essential for bipedal walking. prehensile tails that are useful for locomotion. It is difficult 4. The vertical climbing model to develop a model based on only one or two extant nonhu- Prost (1980) demonstrated that the body movement of man primate species. chimpanzees during vertical climbing was more similar to In arboreal environments, primates developed long and that during bipedal compared with quadrupedal walking. robust limbs, orthograde trunks, and strong hindlimbs, During vertical climbing, the trunk stands vertically, the hip which support and drive the body. Hindlimb-supported near- and knee joints extend strongly, and the ankle joint pushes ly orthograde locomotion in total, including bipedalism and the body powerfully upwards (Yamazaki and Ishida, 1984). quadrupedal climbing, and excluding forelimb suspensory, Muscle activity during vertical climbing also shows more is about 11–26% in wild black-handed spider monkeys resemblance to that during bipedal compared with quadru- (Mittermeier, 1978; Fontaine, 1990). Nearly orthograde lo- pedal walking (Stern and Sussman, 1981; Vangor and Wells, comotion is about 54–59% of arboreal locomotion among 1983). Interestingly, arboreal primates show stronger func- wild adult chimpanzees (Doran, 1993b). In wild adult bono- tional differentiation between the fore- and hindlimbs than bos, nearly orthograde locomotion is about 44–65% of arbo- relatively terrestrial nonhuman primates during vertical real locomotion (Doran, 1993a). In wild adult orangutans, climbing (Hirasaki et al., 2000). Vertical climbing is consid- nearly orthograde locomotion, including quadrupedal clam- ered a part of the preadaptation process for bipedalism. bering, represents around 46–63% of total locomotion in However, the locomotion rate involving true vertical climb- Sumatran orangutans, and about 28–56% in Bornean ones ing—noting that the ascription of locomotor categories (Sugardjito and van Hooff, 1986; Cant, 1987; Thorpe and ‘climbing’ and other related terms can be problematic be- Crompton, 2006; Manduell et al., 2012). cause of different definitions given by individual field ob- The adaptation to arboreal space could therefore be part of servers (Fontaine, 1990)—and not including oblique clam- the preadaptation process for bipedal locomotion. This mod- bering, is relatively small in primates: about 10–16% in wild el is referred to as the ‘generalized arboreal activity model’ black-handed spider monkeys (Mittermeier, 1978; Fontaine, and includes not only single activities, such as orthograde 1990), about 12% in wild adult chimpanzees (Doran, behavior, vertical climbing, or hand-assisted bipedality, but 8 T. KIMURA Anthropological Science focuses on multiple positional behaviors among the three- ments. Its forelimbs were shorter than its hindlimbs, similar dimensional discontinuous environments. Kimura and to the generalized above-branch quadrupedal monkeys and Yaguramaki (2009) suggested the following features of our Proconsul sensu lato; furthermore, no traces of knuckle- pre-bipedal ancestors who could easily initiate and continue walking have been found, and no obvious specializations bipedal locomotion relatively efficiently: relatively erect attributed to forelimb dominant suspension and vertical trunks during locomotion; relatively fixed knee joints; high climbing as in extant African apes (Lovejoy et al., 2009b; activity of the triceps surae muscles at push-off; and high White et al., 2015). potential energy during the single stance-phase. Many of The next human ancestor, Australopithecus, from be- these features are related to the primates associated with tween 2.5 and 4.2 Ma, lost the abducted big toe, but gained arboreal activity among a three-dimensional environment an adducted one for toe-off together with the small toes as- with gaps. In addition, as described and discussed in the sociated with the rocking mechanism of the foot during bi- previous sections, long and robust limbs, extended lower pedal walking, similar to present-day humans (Leakey and limb joints, plantigrade soles, and hindlimb dominance can Hay, 1979; Masao et al., 2016). However, some arboreal also be related to such arboreal activity. Our human ances- adaptations, such as somewhat long upper limbs and long tors preadapted in such environments could have started and ventrally curved hand bones, were retained in its post- more energy-efficient bipedal walking from the first step cranial bones (Susman et al., 1984). Because of the differ- they took when they came down to the ground. ence in body proportions compared with recent humans, the bipedal patterns of Australopithecus could have differed Fossil evidence from those of present-day humans. However, bone morphol- ogy has confirmed that bipedal walking in Australopithecus Does the fossil record agree with the generalized arboreal was not ‘bent-hip, bent-knee’ walking, but rather was per- activity model? Proconsul sensu lato is thought to be the formed while relatively erect with extended lower limb common ancestral hominoid of humans and African apes joints (Lovejoy et al., 1973; Crompton et al., 1998; Lovejoy, from between 17 and 20 Ma. This species utilized general- 2007). ized arboreal quadrupedalism with a pronograde posture but At the around same time, bipedal feet with abducted big not suspension under branches (Walker and Pickford, 1983). toes dating from 3.4 and 3.3 Ma have been discovered in Based on the estimated length of the limb bones, their fore- Ethiopia (Haile-Selassie et al., 2012) and South Africa limbs were likely slightly shorter than their hindlimbs. (Clarke and Tobias, 1995), respectively. Ardipithecus-like Around the same age of between 16 to 18 Ma, Afropithecus locomotion adaptation (Haile-Selassie et al., 2012) could appears to have had similar locomotion adaptations to have persisted for a long time. More detailed discoveries are Proconsul sensu lato (Leakey et al., 1988; Ward, 1998). On waited. the other hand, Morotopithecus were arboreal African homi- Homo erectus sensu lato, which appeared about 1.8 Ma in noids from about 20 Ma that are considered to have relied on Africa, had long lower limbs, relatively short upper limbs, some orthograde positional behaviors such as forelimb sus- and straight and short hand bones (Walker and Leakey, pension and climbing; however, few parts of its postcranial 1993), similar to present-day humans. Their relatively short skeleton have been found (MacLatchy et al., 2000). Follow- upper limbs were lighter, and together with their long lower ing these species, between 14 and 17 Ma, Nacholapithecus, limbs (Steudel-Numbers, 2006), increased efficiency during which were hominoids that lived in the trees, may have had walking. Their locomotion would be fundamentally similar more developed forelimbs and engaged relatively frequently to that of present-day humans. They migrated out of Africa in orthograde behavior such as vertical climbing; however, for the first time in human lineage, likely utilizing their loco- no evidence has been found to suggest a suspensory special- motor ability on the ground, including their long-distance ization (Nakatsukasa, 2004). All of the above hominoids gait. were arboreal locomotors who basically practiced general- The generalized arboreal activity model of human bipedal ized arboreal quadrupedalism and did not obviously special- acquisition presented here is not fundamentally contradicted ize in suspensory locomotion or knuckle-walking, although by the fossil record. In other words, our human ancestors had some hominoids shared traits of orthograde positional be- already preadapted to erect bipedalism in the arboreal envi- havior. Equatorius is an exceptional fossil hominoid that ronment and subsequently refined this process in their terres- practiced semi-terrestrial quadrupedalism in early and mid- trial surroundings. dle Miocene Africa (Sherwood et al., 2002; Patel et al., 2009). No locomotor skeleton fossils from just before and Terrestrial humans after the divergence of the human lineage from African apes have been found, and fossils of locomotor African ape skel- The process described in this review attempts to explain etons after the divergence have rarely been unearthed. how humans acquired erect bipedal locomotion. Compara- Regarding the human lineage after the divergence, tive studies of extant primates have indicated that arboreal 4.4 Ma, Ardipithecus exhibited erect bipedalism on level life is crucial for acquiring bipedalism. Our human ancestors substrates, but with an abducted big toe that was capable of were able to progress to bipedalism because humans belong grasping (Lovejoy et al., 2009a, 2009b; White et al., 2015). to an order of primates that was generally arboreal in nature. This species is thought to have lived in both wooded grass- The fossil record to date supports the hypothesis that our lands and forests. This clearly demonstrates that the bipedal- early bipedal human ancestors lived in the trees. Therefore, ity exhibited by this species started in arboreal environ- the general arboreal activity model of bipedal acquisition Vol. 127, 2019 HOW DID HUMANS ACQUIRE ERECT BIPEDAL WALKING? 9 appears valid. Cant J.G.H. (1987) Positional behavior of female Bornean orangu- The final question of why our human ancestor acquired tans (Pongo pygmaeus). American Journal of Primatology, 12: bipedalism remains unanswered. It is still difficult to answer 71–90. Cartmill M., Lemelin P., and Schmitt D. (2002) Support polygons this question based on the evidence. The local environment and symmetrical gaits in mammals. Zoological Journal of the of Ardipithecus from 4.4 Ma is thought to have ranged from Linnean Society, 136: 401–420. the forest to wooded grasslands (White et al., 2009). Other Cavagna G.A., Thys H., and Zamboni A. (1976) The sources of so-called early humans from around 6 to 7 Ma are consid- external work in level walking and running. Journal of Physi- ered to have lived in environments comprising both grass- ology, 262: 639–657. lands and forests (Pickford and Senut, 2001; Vignaud et al., Cavagna G.A., Heglund N.C., and Taylor C.R. (1977) Mechanical work in terrestrial locomotion: two basic mechanisms for 2002). Present-day African great apes traverse the ground minimizing energy expenditure. American Journal of Physiol- between the trees mainly using quadrupedal locomotion, ogy, 233: R243–261. probably because they have not developed full bipedalism in Clark G. and Henneberg M. (2017) Ardipithecus ramidus and the the trees. Ancestors of relatively terrestrial quadrupedal ex- evolution of language and singing: an early origin for hominin tant primates, such as baboons, might have existed in arbo- vocal capability. Homo, 68: 101–121. real environments, and could have descended from the trees Clarke R.J. and Tobias P.V. (1995) Sterkfontein Member 2 foot bones of the oldest South African hominid. Science, 269: without acquiring the enough bipedal ability at the time and 521–524. adapted to the quadrupedal locomotion on the ground after- Crompton R.H., Li Y., Wang W., Günther M., and Savage R. (1998) wards. By contrast, our human ancestors probably already The mechanical effectiveness of erect and ‘bent-hip, bent- had sufficient bipedal ability in the forest and employed bi- knee’ bipedal walking in Australopithecus afarensis. Journal pedal locomotion from the very first step they took when of Human Evolution, 35: 55–74. they came down to the ground. However, whether our hu- Crompton R.H., Thorpe S., Wang W., Li Y., Payne R., Savage R., Carey T., Aerts P., Van Elsacker L., Hofstetter A., Günther M., man ancestors acquired bipedalism necessarily or contin- and Richardson J. 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