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Journal of Zoology
Journal of Zoology. Print ISSN 0952-8369

Challenges to human uniqueness: bipedalism, birth and brains

A. M. Roberts & S. K. S. Thorpe
University of Birmingham, Birmingham, UK

Keywords knuckle-walking quadrupedalism; orthogrady; bipedalism; obstetric dilemma; altriciality; expensive tissue; metabolic rate. Correspondence Alice M. Roberts, School of Biosciences, University of Birmingham, Edgbaston, Birmingham B15 2TT, UK. Email: roberamy@bham.ac.uk Editor: David Hone Received 4 July 2013; revised 5 November 2013; accepted 11 November 2013 doi:10.1111/jzo.12112

Abstract
Historically, paleoanthropology has focused on explaining human uniqueness. This review paper highlights several recent challenges to key features that have been considered to be exclusive to hominins, testing three long-standing theories in evolutionary anthropology. The knuckle-walking quadrupedalism model describes the evolution of modern gorillines, panins and hominins from a common, knuckle-walking ancestor. But the homology of knuckle-walking in African apes has been questioned. Although habitual bipedalism is unique to humans, it may have developed from occasional bipedalism in ancestors, without a quadrupedal stage. The obstetric dilemma seeks to explain the helplessness of human infants. The timing of human birth is seen as uniquely constrained by fetal head size and maternal pelvic width. An alternative hypothesis suggests that birth occurs when fetal demand for energy threatens to exceed maternal supply; this mechanism also appears to operate in other mammals. The expensive tissue hypothesis suggests that the expansion of energy-hungry brain tissue in hominins was offset by a reduction in gut tissue. But although large brains are correlated with both good quality diets and relatively short guts in primates, the causes of this correlation are not clear. An alternative suggestion is that the large human brain is paid for by savings in other functions, such as locomotion and reproduction, and that a concurrent expansion of low-cost adipose tissue in humans keeps metabolic rate low. In the past, paleoanthropology may have focused on dening a boundary between humans and animals, but recent research has seen a shift of focus to exploring humans as animals. Aspects of bipedalism, birth and brains have been considered to be exclusively human, but in the last few years even these have been eroded. It is the package of features that characterizes Homo sapiens that is unique.

Introduction
Darwin explained human origins in a broad biological context. He was concerned with explaining human traits as predictable and natural results of the general evolutionary process (Cartmill, 1990). This conceptual framework continued to characterize paleoanthropology throughout the rst half of the 20th century, with the study of human evolution theoretically integrated within biology and primatology. But the latter half of the century saw a change of focus, as paleoanthropology sought to explain human uniqueness and to dene the boundary between humans and other animals. The construction of this boundary included the identication of individual, diagnostic human traits, redening these where necessary in order to exclude other animals (Cartmill, 1990; Cartmill & Brown, 2012). However,
Journal of Zoology 292 (2014) 281289 2014 The Zoological Society of London

although the combination of features that characterize Homo sapiens may be unique, comparative studies continue to reveal previously unrecognized similarities between humans and other animals. In this paper, we review recent and signicant challenges to three inuential theories in evolutionary anthropology. The theories being challenged represent perhaps the last bastions of a concept of human uniqueness which identies individual features as unique. In each case, the challenge has appeared in the form of an alternative hypothesis, published within the last 4 years. The long-standing theories are: the knuckle-walking quadrupedalism model; the obstetric dilemma; and the expensive tissue hypothesis. Bipedalism is considered to be the core hominin adaptation, and yet its origins are still debated (Crompton, Sellers & Thorpe, 2010). For decades, the prevailing hypothesis has involved the
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evolution of habitual bipedalism in hominins from a knuckle-walking ancestor (Washburn, 1967; Tuttle, 1974; Wood & Richmond, 2000). Recent fossil discoveries and comparative anatomical studies have cast doubt on this sequence of events (Kivell & Schmidt, 2009; Crompton et al., 2010). Another dening feature of humans is extreme encephalization. The obstetric dilemma focuses on the female pelvis and describes a tension between the demands of bipedalism and giving birth to big-brained babies; the hypothesis seeks to explain the helplessness of human neonates, while proposing a uniquely human mechanism for the timing of parturition (Washburn, 1960; Rosenberg, 1992). Studies of human physiology and biomechanics have led to the suggestion of an alternative explanation for human altriciality (Dunsworth et al., 2012). The expensive tissue hypothesis suggests that, over the course of human evolution, the expansion of the energy-hungry brain was balanced by a reduction in gut tissue (Aiello & Wheeler, 1995). Evidence from anatomical and physiological studies of humans and other mammals has also called this explanation into question (Hladik, Chivers & Pasquet, 1999; Pasquet & Hladik, 2005; Navarrete, van Schaik & Isler, 2011). The challenges to these three theories illustrate how anatomical, physiological and behavioural features that have previously been considered to be uniquely human are shared by other primates or, even more generally, by other mammals.

Origins of bipedalism: the knuckle-walking quadrupedalism model

The most iconic image of human evolution is Rudolph Zallingers illustration for F. Clark Howells book, Early Man, published in 1965. Originally entitled The Road to Homo sapiens, it has become known as The March of Progress. Although Howell (1965) certainly did not describe a linear trajectory of hominin evolution in his text, the linearity of the illustration overwhelmed that message. This single illustration from Howells popular science book has crystallized a widespread misconception, helping to create a concept of human evolution, and evolution more generally, as an uninchingly linear and perhaps even predestined March of Progress (Gould, 1989). The image is very clear about something else: bipedal hominins evolved from a chimpanzee-like, knucklewalking ancestor. Whereas all living apes are capable of bipedality, humans are unique among apes in being habitual bipeds (Preuschoft, 2004; Crompton et al., 2010). This habitual bipedalism has been considered to be an apomorphic behaviour: a dening characteristic of humans and their ancestors. But the origin of such bipedalism in hominins has sparked intense debate (Richmond, Begun & Strait, 2001). In the early 20th century, the prevailing view was that human bipedalism developed from arboreal locomotor behaviour, and in particular, brachiation (Keith, 1923; Avis, 1962). The later 20th century saw a shift: genetic studies placed humans rmly in a clade with knuckle-walking sister taxa (Ruvolo, 1997), suggesting that,
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most parsimoniously, the common ancestor of gorillas, chimpanzees and humans would also have been a knuckle-walker (Washburn, 1967; Tuttle, 1974; Wood & Richmond, 2000). Many researchers have also argued that extant African apes, humans and fossil hominins share particular osteological features, especially in the hand and wrist, which relate to knuckle-walking (Tuttle, 1969; Corruccini, 1978; Gebo, 1996; Richmond & Strait, 2000, 2001; Corruccini & McHenry, 2001; Richmond et al., 2001). This knuckle-walking quadrupedalism model relies on the homology of knuckle-walking in chimpanzees and gorillas, but several studies have cast doubt on this interpretation (Dainton & Macho, 1999; Dainton, 2001). Proposed links between knuckle-walking and particular anatomical features (e.g. scaphoid-centrale fusion) in extant apes have been questioned (Kivell & Schmidt, 2009). It has been argued that the suggested knuckle-walking features of hominoids, including those contributing to stability at the wrist joint (e.g. the angulation between scaphoid and lunate facets of the distal radius), may be better interpreted as adaptations to arboreal locomotor modes, such as vertical climbing (Dainton, 2001; Kivell & Schmidt, 2009). The discovery and analysis of Ardipithecus ramidus has provided another challenge to the knuckle-walking quadrupedalism model. The anatomy of this 4.4 million-year-old hominin suggests that its locomotor pattern included terrestrial bipedalism combined with above-branch palmigrade/ plantigrade arboreal quadrupedalism (Lovejoy et al., 2009; Lovejoy & McCollum, 2010). However, Crompton et al. (2010) argued that Ardipithecus is unlikely to have been an arboreal above-branch quadruped, given its stiff, noncompliant feet and large body size. While there is debate about how Ardipithecus may have moved in trees, there is general agreement that this species was terrestrially bipedal, with no evidence for knuckle-walking in its locomotor repertoire, nor any evidence that it evolved from an earlier knuckle-walking ancestor (Crompton et al., 2010). If terrestrial knuckle-walking quadrupedalism was not the precursor of terrestrial bipedalism in hominins, the possibility of an arboreal origin for bipedalism should be re-examined. In his hylobatian model, Keith (1923) suggested that skeletal features shared by the apes (e.g. broad ilia; broad, shallow trunks; dorsally placed scapulae), which contrast with features characteristic of quadrupeds (e.g. rod-like ilia; narrow, deep trunks; laterally placed scapulae), arose because of the adoption of an upright body posture for arm-swinging, forelimbsuspensory locomotion in small-bodied ape forerunners similar to living gibbons. Later, Tuttle developed his own hylobatian model that focused on vertical climbing as the precursor to human bipedalism (Fleagle et al., 1981; Tuttle, 1981). Modern chimpanzees and gorillas vertically climb tree trunks with ease. But this type of climbing, like knucklewalking, involves highly exed hips and knees; in vertical climbing in apes, the hip never extends as far as it does during human bipedalism (Crompton et al., 2003). In contrast, human bipedalism is characterized by extended limb postures (Alexander, 1991, 2004). Although a bent-hip-bent-knee type of bipedalism might be seen as a reasonable intermediate step
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Challenges to human uniqueness

here, just as in the knuckle-walking quadrupedalism model, it seems both anatomically and energetically unlikely that early hominins such as Australopithecus afarensis could have walked long distances in this way, and much more likely that they already walked with extended lower limbs (Carey & Crompton, 2005; Lovejoy & McCollum, 2010). Tuttles hylobatian model included another mode of arboreal locomotion: bipedalism along horizontal boughs. This is part of the locomotor repertoire of large-bodied great apes today (Hunt, 1991; Thorpe & Crompton, 2006). Among the great apes, the orangutan is the most bipedal and the most arboreal (Thorpe & Crompton, 2006; Crompton et al., 2010). The bipedalism of orangutans is also biomechanically closest to that of humans (Crompton et al., 2003). Although only 8% of orangutan arboreal locomotion is bipedal (Thorpe & Crompton, 2006), it is functionally important: orangutans stand on two legs to access the terminal branch niche. They support themselves on slender branches to reach fruits at the periphery of trees, and to bridge between trees without having to climb down and back up again (Crompton et al., 2003; Thorpe, Holder & Crompton, 2007). Long limbs, offering an extended reach and easy bridging of gaps, could even predispose an ape towards arboreal bipedalism, favouring an upright trunk, with long legs brought under the bodys centre of mass (Preuschoft, 2004). Compressive orthogrady may also characterize vertical, as well as horizontal, movement within trees: extant apes, particularly the orangutan, engage in orthograde clamber (Thorpe & Crompton, 2006). This type of clambering, involving extended hind-limb postures, may represent both a more plausible accompaniment and precursor to bipedalism than vertical climbing (Thorpe et al., 2007). Crompton et al. (2010) argued that compressive orthogrady may have been important within the arboreal locomotor repertoire of several species of Miocene ape, including Pierolapithecus, Hispanopithecus and Morotopithecus. It seems that at least one Miocene ape may also have been regularly bipedal on the ground. Oreopithecus bambolii, dating between 7 and 9 May, possesses a few characters, including a bicondylar angle at the knee, together with hips and knees adapted for use in extension, that suggest this species was not only orthograde, but terrestrially bipedal (Crompton, Vereecke & Thorpe, 2008). A. ramidus may have moved in a similar way, combining arboreal compressive orthogrady (rather than arboreal quadrupedalism) with terrestrial bipedalism (Crompton et al., 2010). Amidst continuing debate, there is therefore a growing body of evidence supporting an arboreal origin for human bipedalism. Recent studies have reinvigorated the idea that the origin of hominin terrestrial bipedalism was arboreal, rather than emerging, when a terrestrial quadruped stood up to become a biped (Kivell & Schmidt, 2009). Compressive orthogrady, in the form of clambering and arboreal bipedalism, is a biomechanically plausible precursor of terrestrial bipedalism, and remains part of the arboreal locomotor repertoire of hominoids today, particularly in orangutans and humans. Adaptations to terrestrial bipedalism, and a range of different types of bipedalism, may have arisen before the
Journal of Zoology 292 (2014) 281289 2014 The Zoological Society of London

separation of hominins and panins, and may not have been limited only to hominin ancestors. Among extant species, regular terrestrial bipedalism is a special characteristic of a single ape species: H. sapiens. But taking the long view, and as Thorpe et al. (2007) suggested, it seems increasingly probable that the ancestors of chimpanzees and gorillas independently developed the innovation of knuckle-walking, while human bipedalism was the conservative option.

Birth and brain size: the obstetric dilemma

Whereas most primates are highly developed at birth, human babies are born helpless (Rosenberg & Trevathan, 2002). Human altriciality has important implications for human society and behaviour: helpless infants are cared for through pair-bonding, and by grandparents and other alloparents. The obstetric dilemma suggests that two dening characteristics of humans have interacted to force infants to be born at an early stage of neurological and cognitive development: human pelves are limited in width by the functional constraints of bipedalism, and babies must be born before their heads grow too large for the birth canal (Rosenberg, 1992; Rosenberg & Trevathan, 2002). While chimpanzees are born with brains around 40% of adult size, the human neonate brain is only 30% of adult size (DeSilva & Lesnik, 2008). Although some authors have suggested that the extreme altriciality of human infants could be adaptive, guaranteeing intensive contact with parents and enhancing opportunities for social learning (van Schaik & Burkart, 2011), the obstetric dilemma suggested that it is an unavoidable consequence of competing demands from selection for bipedalism and for large adult brains (Washburn, 1960; Rosenberg, 1992; Dunsworth et al., 2012). Theres an implicit assumption in the obstetric dilemma that the narrower human male pelvis is better suited to the mechanical demands of bipedalism, and that the wider female pelvis is compromised (Dunsworth et al., 2012). In a wide female pelvis, the hip abductors on the stance leg, during walking or running, should have to work harder to keep the pelvis horizontal. However, several studies of the metabolic cost of walking and running have shown women to be just as economical as men (Bourdin et al., 1993; Hall et al., 2004), indicating that these biomechanical costs do not translate into increased energetic demands. Analysis of dynamic forces during walking and running suggests that the potential cost of a broader pelvis may be offset by subtle adjustments in the movement of other segments (leg and foot) during walking and running (Dunsworth et al., 2012). These studies of the metabolic cost and dynamics of bipedal locomotion suggest that the relatively wide pelvis of human females does not compromise locomotor efciency. The wide range of variability in both neonatal brain size and pelvic dimensions also makes it unlikely that the female pelvis has been subject to strong locomotor constraints (Wells, DeSilva & Stock, 2012). The shape of early hominin pelves has been interpreted as representing adaptations to habitual bipedal locomotion. The
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australopithecine pelvis displays several such adaptations, including positioning of the anterior gluteal muscles lateral to the hip joint, reduced iliac height, and retroauricular expansion of the ilium to reposition gluteus maximus (Lovejoy, 2005). Changes to pelvic structure in later hominins, including an absolute increase in coronal width, and a relative increase in sagittal depth, have been interpreted as adaptations to giving birth to large-brained babies (Lovejoy, 2005). However, partial pelves from two Australopithecus sediba individuals appear to show that some derived Homo-like features, including a relatively large sagittal diameter and upward rotation of the pubis, emerged before signicant expansion in brain size occurred. It may be that some features that have been previously linked to obstetric demands in Homo may instead reect altered locomotor demands on the pelvis, at least in A. sediba. Nevertheless, the pelvis of Homo still presents features, including an absolute increase in coronal width, which are likely to be related to birthing big-brained babies (Kibii et al., 2011). The parity in efciency of locomotion in men and women today, the variability of modern female pelves, and the changes in the hominin pelvis accompanying encephalization in Homo suggest that the pelvis is unlikely to have placed an evolutionary constraint on the maximum size of the neonatal head, and therefore upon the length of gestation (Lovejoy, 2005; Dunsworth et al., 2012). In many mammals, including primates, the length of gestation appears to be limited by the energetic demand of the fetus in relation to maternal provision (Martin, 1996; Dunsworth et al., 2012). Although the precise mechanism for timing human birth remains elusive, and has been called the greatest unresolved question in reproductive biology (Plunkett et al., 2011), the maternal or metabolic crossover hypothesis (Ellison, 2001) suggests that parturition occurs when the energy demands of the fetus threaten to exceed maternal capacity for supply. During pregnancy, a human mothers metabolic rate rises to twice her basal metabolic rate (BMR); by 9 months, fetal demand pushes maternal energy requirements close to 2.1 BMR, and this coincides with the end of gestation (Dunsworth et al., 2012) (Fig. 1). While the length of gestation may be limited by energetics rather than the dimensions of the maternal pelvis (Dunsworth et al., 2012; Wells et al., 2012), this fails to explain why childbirth is difcult and potentially dangerous in modern humans (Rosenberg, 1992). Humans are not alone in experiencing difculty during childbirth (Rosenberg & Trevathan, 2002). Non-human apes have wide pelves, and childbirth tends to be easy, but in most monkeys, especially marmosets and squirrel monkeys, the maternal pelvis is only slightly larger than the fetal head (Schultz, 1949; Rosenberg, 1992). However, human parturition is a longer and apparently more painful process than it is in other primates (Rosenberg, 1992). Cephalopelvic disproportion can result in obstructed labour (dystocia), placing both the mother and babys lives at risk (Maharaj, 2010). Although, in most human societies, mothers seek company and assistance during childbirth (Rosenberg, 1992; Rosenberg & Trevathan, 2002), dystocia is still a signicant problem. The worldwide incidence of dystocia is estimated to be 36% (Dolea & AbouZahr, 2003), while a recent study in
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Offspring energy requirement or additional maternal energy requirement (kcal/day)

1000 900 800 700 600

Maximum sustainable metabolic rate

2.3 2.2 2.1 2.0

Total maternal energy requirement / BMR

500 400 300 200 100 0 0 5 10 15 20 25 BIRTH 1.9 1.8 1.7 1.6

Months post-conception
Figure 1 Metabolic constraint on gestation length. Maternal energy expenditure (grey squares) and fetal energy demands (black circles): birth occurs before maternal energy requirement rises to 2.1 BMR (Dunsworth et al., 2012). (Graph reproduced with kind permission from the authors.)

West Africa found the incidence to be as high as 18% (Ould El Joud et al., 2001). An anatomical predisposition to dystocia would be expected to reduce evolutionary tness, so it may be that the obstetric dilemma can offer an explanation for difcult childbirth in contemporary human populations. It is possible that locomotor constraints are producing a selective pressure that precludes any further increase in pelvic width (Dunsworth et al., 2012). However, the suggestion of an evolutionary pay-off between locomotor function and reproductive success is problematic. The consequences of a pelvis too narrow to birth a baby would far outweigh any locomotor disadvantage: natural selection is unlikely to have produced a constraint on pelvic width which would so effectively reduce reproductive success (Roy, 2003; Lovejoy, 2005; Wells et al., 2012). It is possible that difculty in childbirth is a very recent phenomenon (Roy, 2003; Dunsworth et al., 2012). Although there are very little robust data, anecdotal evidence suggests that dystocia is very rare among contemporary hunter gatherers (Roy, 2003), and evidence for dystocia is also rare in the archaeological record (Wells et al., 2012). In contrast, dystocia is a major cause of maternal mortality in contemporary agricultural communities in developing countries, where childhood malnutrition is common (leading to short stature and small pelvic dimensions in adulthood), and where women have limited access to obstetric care (Wittman & Wall, 2007; Wells et al., 2012). Dystocia is much less common, but neither is it rare, in afuent societies. Here, the problem could lie in a relatively rapid improvement in nutrition (Roy, 2003), particularly with mothers consuming a diet with a high glycaemic index, associated with macrosomia (excessive birth weight) in infants (Wells et al., 2012). While it is likely that high rates of dystocia and poor outcomes for mothers and infants will be creating selection pressure in developing countries, there is little selection pressure against small pelves in countries where
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women have access to obstetric care, and where mothers and babies survive even when cephalopelvic disproportion makes vaginal delivery impossible. In conclusion, it seems likely that human gestation length is limited by energetics rather than the size of the maternal pelvis. The hominin pelvis has grown wider to accommodate an expanding fetal head, and does not appear to have reached a point where locomotion places a constraint on width. Dystocia in contemporary populations may be linked to recent changes in diet, where natural selection has either not had time to adjust pelvic size, or has been circumvented by obstetric intervention.

Bowels and brains: the expensive tissue hypothesis

Humans appear to be truly unique in the extent of their capacity for copying, cooperation and culture (Whiten, 2011). Large brains have underpinned our success as a species: culture and technology have enabled humans to survive in a huge range of environments, and have supported phenomenal population growth. But brains are energy-hungry organs, and the average 65-kg human has a brain a full kilogram larger than expected for a standard mammal of that body mass at 1.3 kg. The metabolic rate of brain tissue is over 11 W kg1, while the average metabolic rate of the human body is just over 1 W kg1. The extra kilogram of brain should cost the human body an extra 12 W, but there is no evidence of raised BMR to accommodate this: BMR in humans is exactly what would be expected for a mammal of comparable body mass (Aiello & Wheeler, 1995). The expensive tissue hypothesis suggested that the expansion of the brain could have been compensated for by a reduction in energy-hungry tissue elsewhere. Aiello & Wheeler (1995) suggested that, while the heart, kidneys and liver were close to the expected size for a 65-kg primate, the human gut was considerably smaller at about 60% of expected size. The hypothesis suggested a coevolution between brain size and gut size such that expansion in one would be matched by a reduction in the other, in order to maintain a typical BMR. The reduction in gut size was linked to a higher quality diet, with the inclusion of meat in early hominin diets, and cooking providing another potential energy saving after the origin of Homo (Aiello & Wheeler, 1995). Aiello & Wheeler (1995) noted that previous authors had recognized a relationship between diet and brain size, explaining this in terms of relative intelligence, the leaves of a folivores diet being somewhat easier to outwit than the more animate components of an omnivores diet. As folivores have longer guts than omnivores, this produces an inverse relationship between gut size and brain size. But Aiello & Wheeler (1995) saw energetics as providing a better explanation, arguing that a high-quality diet was necessary for encephalization via a reduction in the size and energetic demand of the gut. At the time of publication, several authors submitted comments to Current Anthropology. Both Armstrong and
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Wrangham, Holland & Leighton (in Aiello & Wheeler, 1995) observed that the hypothesis would be strengthened if a similar relationship between gut size and brain size were to be discovered in other taxa. Falk (in Aiello & Wheeler, 1995) commented that the expensive tissue hypothesis did not suggest a prime mover for brain expansion, but rather provided a prime releaser or, as Henneberg (in Aiello & Wheeler, 1995) commented, a conditio sine qua non. Henneberg also raised a concern about presenting data for a standard human, given wide ranges of anatomical variation among living humans, and pointed out that the proposed energy saving could have been achieved in many other ways, being equivalent to a 45-min walk, 6.8 kg of body mass, a few degrees of difference in ambient temperature or a little more sleep. Henneberg suggested that the structural reduction of the human body in the late Pleistocene, as technology supplemented biological functionality, might provide a more likely compensator for bigger brains. Milton (in Aiello & Wheeler, 1995) turned the hypothesis on its head, offering perhaps a more evolutionarily plausible explanation, arguing that the brain may have expanded to provide the necessary foraging skills to secure a high-quality diet, and that the gut may have shrunk as a result. She made the point that it would be evolutionarily irresponsible to cast off gut tissue until mental complexity was sufciently developed to . . . ensure dietary quality (Milton, in Aiello & Wheeler, 1995). Several subsequent studies have tested the predictions of the expensive tissue hypothesis in primates and other animals. A study examining the relationship between diet quality and brain mass in non-human primates found a signicant positive correlation, which was argued to provide support for the expensive tissue hypothesis (Fish & Lockwood, 2003). But although good quality diets are usually associated with shorter, less complex guts, and good quality diets are also usually associated with larger brains, this does not mean that gut reduction is necessary for encephalization. A switch to a higher quality diet alone could provide the necessary energy, and Hennebergs (in Aiello & Wheeler, 1995) criticisms still stand: the extra energy could be gained elsewhere. Miltons (in Aiello & Wheeler, 1995) comments are also relevant: brain expansion could have facilitated the acquisition of highquality foods with gut reduction as a consequence. A study published in 2003 claimed to provide independent support for the expensive tissue hypothesis based on studies of brain and gut sizes in sh (Kaufman, 2003). Among three species (the carnivorous African sh Gnathonemus petersii, the carnivorous Southeast Asian sh Chitala chitala, and the South American herbivorous species Hypostomus plecostomus), the relative masses of the gut and brain were negatively correlated. In a reply to this short paper, Hladik & Pasquet (in Kaufman, 2003) pointed out that, within insectivores and primates, large variations in diet existed within groups that differ widely in terms of brain size, so that dietary adaptations appear to be totally independent of brain size. They further suggested, echoing Miltons (in Aiello & Wheeler, 1995) criticism of the original hypothesis, that a sh species that hunts (G. petersii) could be expected to have a larger brain.
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Another study focused on bats, testing the prediction of the expensive tissue hypothesis that relative brain mass would exhibit a negative correlation with relative gut size. Among bats, non-fruit-eating bats, most of which are insectivores, have relatively smaller brains than fruit-eating bats. The expansion of the brain in the fruit-eating bats is largely due to an increase of visual and olfactory areas, supporting the acquisition of fruit. The study found a positive correlation between brain size and gut size in bats, and the authors argued that this challenged the general applicability of the expensive tissue hypothesis (Jones & MacLarnon, 2004). This study demonstrates how difcult it is to extrapolate ndings in one group of mammals to others where diets and means of food acquisition vary. Aiello & Wheeler (1995) accepted that their small dataset was not ideal, but they argued that the general patterns, particularly the inverse relationship between brain and gut sizes, were dependable. However, while the broad distinction between larger brained frugivores and smaller brained folivores may be generally true for primates, it is not clear that humans do possess a relatively small gut. Hladik et al. (1999) suggested that the predicted gut size for humans (as omnivores) may have been overestimated, as this prediction was based on a sample of non-human primates which included folivorous species. In addition, the same authors argued that gut area was a more meaningful measure than mass. The relative gut area of mammals reects quality of diet: animals eating high-quality diets, containing animal protein, tend to have smaller guts, whereas those consuming low-quality diets tend to have relatively large guts. Plotted onto a graph for the three major diet types of mammals [folivore/ frugivore(omnivore)/faunivore], humans fall on the frugivore (omnivore) axis, as expected for an ape (Hladik et al., 1999; Hladik & Pasquet, 2002; Pasquet & Hladik, 2005). Even without gut reduction, switching dietary focus to include highquality foods (such as meat or, indeed, fruit and tubers) could have yielded the energy needed for large brains in early Homo both by increasing energy intake and by reducing the day range necessary for foraging (Hladik et al., 1999). Cooking and other means of food processing could also have played a signicant role in improving the energy gain from food (Carmody & Wrangham, 2009) (Fig. 2). Criticisms of the expensive tissue hypothesis, and of subsequent studies that have claimed to provide evidence to support it, have focussed on other potential sources for the extra energy needed by a large brain. However, as Aiello & Wheeler (1995) wrote in response to the comments on their original paper in Current Anthropology: [the] central point remains valid; humans possess a relatively large brain and a relatively small gut and also have no corresponding increase in BMR. A recent study tested the expensive tissue hypothesis against new data: 191 specimens from 100 mammalian species, including non-human primates (Navarrete et al., 2011). This study found no correlation between brain size and the sizes of any other expensive organs, refuting the expensive tissue hypothesis as a general principle among mammals, although humans were not included in the sample. However, the data revealed a negative correlation between brain size and body
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Figure 2 Size of gut (as area of absorptive mucosa) in relation to body size. This relationship reects three major dietary tendencies among primates and other mammals; human specimens fall on the frugivore axis (Hladik et al., 1999). (Graph reproduced with kind permission from the authors.)

fat. The authors suggested that both encephalization and fat storage could be viewed as alternative buffering strategies against starvation (Navarrete et al., 2011). This balance between fat stores and brain tissue could be due to a trade-off: although fat has a low metabolic rate, it may increase the cost of locomotion and make an animal more vulnerable to predation. Fat could also provide the answer to the human BMR conundrum. Humans have larger fat depots than chimpanzees and bonobos, and this low-cost tissue appears to be masking the effect of investing in a large, energy-hungry brain: relative to fat-free body mass, human BMR is higher than in chimpanzees and bonobos (Aiello & Wells, 2002; Navarrete et al., 2011). The extra energy required by large brains in humans could derive from a higher energy input, through increased diet quality, or from energy savings in other areas such as locomotion and reproduction (Navarrete et al., 2011). There appears to be a trade-off between locomotor costs and brain mass in birds, and a similar trade-off could have operated in human evolution (Isler & van Schaik, 2006) (Fig. 3). This new research suggests that humans are likely to have paid for their expensive brains by an increase in net energy intake, as well as energy savings in functions like reproduction and locomotion, maintaining a typical BMR through a relative increase in body fat (Navarrete et al., 2011). The human
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Challenges to human uniqueness

from dening a boundary between humans and animals towards understanding humans as animals, and human evolution becomes conuent with the history of life in general (Cartmill, 1990).

References
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Figure 3 The expensive brain framework. Energy for an expanding human brain could come from an increase in net energy input or reallocation from savings in other functions (Navarrete et al., 2011). (Diagram reproduced with kind permission from the authors.)

gut, rather than representing a peculiar specialization to an unusual diet for an ape, may instead represent something much more mundane, as the gut of an unspecialised frugivore, which now supports a wide range of dietary exibility, from vegetarian to almost exclusively carnivorous (Hladik et al., 1999).

Conclusion
The recent challenges to each of these hypotheses the knuckle-walking quadrupedalism model, the obstetric dilemma and the expensive tissue hypothesis seem disparate, but they are united by a theme: humans are less unique than previously thought. Doubts about the homology of knuckle-walking in chimpanzees and gorillas, as well as evidence showing the importance of arboreal bipedalism to extant apes, have reinvigorated the idea of an arboreal origin for human bipedalism. Regular, terrestrial bipedalism may not be an apomorphic hominin trait, if indeed earlier apes such as O. bambolii behaved in this way. Heretically, the ancestors of knucklewalking chimpanzees and gorillas could even have been regular, terrestrial bipeds a hypothesis that is not yet refuted by the fossil evidence. Human gestation length may be limited by the balance between maternal and fetal energetics, a mechanism that is likely to act in other mammals, rather than through the uniquely human mechanism suggested by the obstetric dilemma. The expensive tissue hypothesis emphasized the importance of energetics in human evolution, and yet the trade-off between brain size and gut size that it proposed now seems too simple. While the human brain remains a remarkable organ, our guts are those of a regular fruit-eating ape, and we are likely to pay for our large brains in a variety of ways. We suggest that such challenges to long-standing hypotheses, relating to the uniqueness of H. sapiens, may represent a philosophical return to the original theoretical context of the discipline. If this is true, paleoanthropology is shifting away
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