The Homo genus originated in Africa around 2-3 million years ago (mya), as the lineage split from the Australopithecine line (Henke and Hardt 2011), the following wide-spread dispersal lead to the colonisation of almost every habitat on Earth as we see today. It is thought that Australopethicines adaptations were confined to habitats in Africa by ecological, physical or climatic reasons, and the adaptations of the Homo species were able to overcome this (Henke and Hardt 2011).
It is possible that the evolution of bipedalism allowed for this rapid expansion. Bipedalism (Latin: Bi = two Ped = feet) is a locomotion strategy of walking on the two rear limbs, a behaviour that is unique among living taxa to H. sapiens (Polk 2004). There are a few indications that the earliest known hominids were bipeds, with fossil evidence showing that Australopethicines habitually walked at around 4.4 mya (Bramble and Lieberman 2004). The evolution of bipedalism led to a large amount of morphological changes in the muscular-skeletal anatomy of Hominid species that improved the energy use in walking by about 75% compared to quadrupedal and bipedal walking in chimpanzees (Bramble and Lieberman 2004). Our closest hominid relative Homo neanderthalensis was a fully biped hominid. This article will compare the musculoskeletal anatomy of Homo neanderthalensis and Homo sapien.
The process of walking
It is important to first describe the process of bipedalism and locomotion in modern humans before comparison between humans and Neanderthals can be achieved successfully, as an understanding of both the bones and muscles involved is required.
The hominid lower limb consists of a femur, patella, tibia & fibula, tarsals, metatarsals and phalanges. Humans exhibit a number of specialisations to these bones and surrounding muscles for bipedalism. Such as, the elongation of the heel and enlargement of the knee joint for weight bearing and an increase in leg length to improve muscular efficiency during walking (Harcourt-Smith and Aiello 2004).
Figure 1. The skeletal anatomy of the leg
The femur evolved to angle medially which keeps the centre of mass above the feet and allows for locking of the knees for standing with little muscular effort (Aiello et al. 1990). Humans are able to walk by the coordination of alternating activity of the extensor and flexor muscles in the leg (Ogihara and Yamazaki 2001). Forces to balance and propel the body forward must be produced simultaneously (Lipfert et al. 2014).
Walking is composed of two distinct phases (Figure 2.) – the stance phase, when the foot is in contact with the ground and the swing phase, when the foot is swung past the other ankle, which is in stance phase and planted onto the ground ahead of the ankle (Hughes and Jacobs 1979). This method Is know as an ‘inverted pendulum’ where the centre of mass vaults over the extended leg during stance phase, efficiently transferring between potential and kinetic energy with every step (Bramble and Lieberman 2004).
Figure 2. The two phases of walking, collectively known ad the gait cycle
Winter and Yack in the late 1980s used electromyography to measure activity of the muscles involved in human walking, it was found that the ‘weight-accepting muscles’ (such as; tibialis anterior, gluteus maximus and medius) were most active in the first bit of the stride to control the forward movement of the trunk. Plantar-flexor muscles were most active at push-off of the ankle while peroneus longus was active at flat-foot to control foot inversion. During swing phase the hip extensors and knee flexors are most active to arrest the forward movement of the lower limb. Adductor longus and magnus act to stabilise the hip joint and are most active during swing phase. On a stride-to-stride basis the knee and hip muscles prevent collapse of the limb in stance phase and correct posture to keep the body weight above the centre of mass, the distal support muscles are also among the most active (Winter and Yack 1986).
While muscles pull in a linear direction their action is always rotational around an axis or joint, the moment is the distance between the line of action of the muscle and the centre of rotation, the larger the moment arm the larger the mechanical advantage. Think about how it is easier to open a door if you’re pushing at the handle and harder when pushing closer to the hinges. (Figure 3.).
Figure 3. The rotational pull of a muscle around the joint. As a larger moment arm gives a better mechanical advantage, in this example B will require less force to move the lower part.
The origin of the Neanderthal
In 1856 a strange human looking skeleton was discovered in the Neander valley, Germany, by a group of quarrymen. After concluding this skeleton was of bear origin it was passed on to scientists and found its way into the hands of William King, an Irish anatomist. It was obvious to King that these were hominid remains but not of H. sapien origin. King (1864) concluded that the fossil remains were in fact that of a distant human relative and proposed the name ‘Homo neanderthalensis, commonly referred to as a ‘Neanderthal’. The skull was long and peculiarly flattened on top and had prominent brow ridges (a defining feature in modern reconstructions), with an estimated brain size of about 1,300 ml (modern humans are 1,200-1,500 ml) (Stringer and Gamble 1993). The pelvis was also unusual and the overall body was strongly built by today’s standards, but not very tall, with a large barrel-shaped chest and a long back. They also had relatively short lower limbs, leading to a short-stocky physique overall (Figure 4.). Neanderthals spanned much of western Eurasia, from as far north west as Britain to south of Israel, during the Late and Middle Pleistocene about 130-40 thousand years ago (kya), with fossils found in a range of environments, most often in colder climates.
Figure 4. The skeleton of the Neanderthal (left) in comparison to the H. sapien skeleton (right) (Straus and Cave 1957)
The fossil record indicates that H. sapiens, evolved in African between 150 and 50 kya (Klein 1995), though it is thought that modern cognitively developed H. sapiens did not appear until around 50 kya shown as the incidence of ornaments, ivory tools and hunter-gatherer innovations, or more succinctly; the appearance of culture. This happened at a time when Neanderthals were the sole hominid inhabitants of Eurasia (Klein 1995). These cognitively developed H. sapiens spread out and inhabited most of the world. While it may at first seem obvious to conclude that a more cognitively developed H. sapien would simply out compete the more primitive Neanderthal, research has shown that Neanderthals were also capable of ‘modern’ behaviour, by the evidence of projectile usage, ornaments and the burying of dead (Stringer and Gamble 1993). So what actually led to the demise of the Neanderthals that once dominated Eurasia?
The unlucky fate of the Neanderthals and the origin of modern humans has been a fundamental debate in evolutionary science research over the last century (White et al. 2003). Since the discovery of H. neanderthalensis in the mid 19th century there has been continuous research and study yielding an unmatched accumulation of data (Hublin 2009). Despite this, there are a number of contrasting theories as to why the Neanderthals went extinct, which are hotly debated.
This article is intended to explore the comparative anatomy of the thigh and leg of Neanderthals and humans to discuss the theory that differences in bipedal locomotion energy efficiencies (that is how costly is it to walk or run) led to the demise of Neanderthals.
It is important to note that one theory states that Neanderthals went extinct about 10,000 years prior to previously thought meaning that Neanderthals and H. sapiens never interacted at all (Higham et al. 2014), however a population model by Mellars in 2004, implies that the extinction of Neanderthals coincided with the emergence of modern humans about 30-40 kya suggesting that interactions were inevitable and may have lead to competitive exclusion of Neanderthals by H. sapiens, this is something that is supported by some researchers (Banks et al. 2008).
Competition occurs when two or more species are limited by the same resource. The theory of competitive exclusion suggests that when the shared resource is in limited supply the ‘better’ adapted species with outcompete the ‘lesser’ adapted species, leading to the extinction of the lesser species. This article will also assess the morphology of the leg and its affect on locomotion efficiency as a possible cause for Neanderthal extinction by non-violent competitive exclusion. Improved locomotion efficiency would make the species a better competitor by improving performance in hunting prey, running from predators and could require less energy for equal or greater activities.
Following Sawyer and Maley’s (2005) unprecedented attempt to reconstruct the entire articulated skeleton of H. neanderthalensis (Figure 5.), a number of observations shed some light on the distinction between modern humans and Neanderthals. In particular, the articulated skeleton enables better understanding of the anatomical relationships that influence posture and overall stature allowing for critical inferences and locomotion analyses. The Neanderthal skeleton was much more robust than H. sapien. The knee joint was particularly large and the walls of the leg bones were very thick (Stringer and Gamble 1993). Large and deep muscle attachment sites are also visible suggesting that Neanderthals were much stronger than H. sapien.
Figure 5. Full articulated Neanderthal skeleton, anterior (left) and lateral profile (right) (Sawyer and Maley 2005).
This raises two possibilities; that H. sapiens did the same activities but at a greater muscular efficiency, needing smaller muscles or that they did less of the activities Neanderthals did. In a study by Chapman et al. (2010) a model Neanderthal leg was generated using computer software to assess the biomechanics of walking and accurate motion analysis. It was found that robustness was proportional to mechanical advantage in the hamstrings and interestingly, was greater than in H. sapien. Concluding that Neanderthals may have had greater bending moments, larger moment arms and overall greater mechanical efficiencies when compared to modern humans, though it is suggested that the greater robustness and muscle mass could have led to fatigue during locomotion (Stringer and Gamble 1993).
One important observation from Sawyer and Maley’s (2005) articulated skeleton is that Neanderthals had relatively shorter tibiae than H. sapiens at approximately 55% of femur length (compared to 85% in H. sapien, Trinkaus 1981). Polk (2002) observed that animals with relatively longer tibiae used more extended knee postures which resulted in less muscular force needed to maintain limb posture and animals with longer tibiae could achieve longer strides and faster speeds. A study by Steudel-numbers and Tilkens in 2004 tested the affect of tibia length on locomotion efficiency to determine energetic differences. The energy cost during a four-minute walk on a treadmill and tibial length of 21 human subjects was measured; finding that shorter tibiae resulted in increased energy consumption. As a result, it can be concluded that Neanderthals were likely to require greater energetic effort for equal locomotion. Some estimates have suggested that Neanderthals were likely to have been heavier and Steudel in the early 90s found that body mass has a significant affect on locomotion efficiency.
Therefore, it is calculated that the cost of locomotion for Neanderthals would be around 30% greater to cover the same distance as H. sapien (Steudel-Numbers and Tilkens 2004). In such a time when Neanderthals and H. sapiens co-existed it is safe to assume that diet and caloric availability would have been very limiting. Thus, significantly improved efficiency in locomotion would have given the H. sapien a huge competitive advantage. A number of researchers, however, argue that shorter tibiae may have been advantageous by reducing the energetic cost of walking due to lower moments of inertia (Holliday and Falsetti 1995, Kramer 1999, Kramer & Eck 2000).
During the time period Neanderthals were alive their shorter tibiae were not selected against (Steudel-Numbers and Tilkens 2004), this allows us to conclude that relatively shorter tibiae conferred some advantage. It is widely accepted that the Neanderthal limb is developed for cold adaption (Trinkaus 1981, Trinkaus 1986, Holliday 1997), and their leg is comparative of modern human Eskimo proportions (Stringer and Gamble 1993). Their ‘barrel-shaped’ chest, would also give a better surface area to volume ratio, reducing heat loss and increasing activity levels in colder climates (Saywer and Maley 2005). Another theory suggests that their shorter tibiae length gave greater muscular power in their legs, Schmitt et al. (2003) suggested that Neanderthals hunted with thrusting spears for which powerful lower limbs could improve their hunting efficiency when engaging prey directly.
Different limb postures can lead to significant differences in costs and benefits of energy expenditure when walking and standing. Biewener (1989) found that extended limb posture could reduce muscular forces required to support the more upright limbs reducing the energy cost of standing. An extended posture may also permit longer strides and require less muscular effort to resist ground reaction forces that would cause the leg to collapse (Gray 1968).
However, longer limbs require more energy to move through the ‘swing phase’ (Polk 2004) and extension requires flexion before jumping is possible, reducing reaction times. Polk (2002) found that both body size and limb proportions can affect joint posture during terrestrial locomotion and concluded that more extended limb postures increased the effective mechanical advantage of limb extensor musculature, particularly at the knee. It is interesting to note that a shorter tibia resulted in a more flexed posture, increasing the moment arm for the ground reaction forces about the joint, thus requiring greater extensor muscular force to prevent joint leg collapse (Figure 6.) (Polk 2004).
Figure 6. The result of limb length and posture on the force required by extensor muscles to stop the leg collapsing due to ground reaction forces. A – longer tibiae length in a flexed posture increases the moment arm and requires greater muscular effort (represent by the arrow). B – a more extended posture reduces the moment arm, thus, reducing muscular effort required to prevent leg collapse (Polk 2004).
This may help to explain the greater muscular masses seen in the Neanderthal skeleton. However, a study by Gatesy and Biewener in 2009 found that living bipeds with a more flexed posture and relatively longer feet (as seen in Neanderthals) allowed for longer relative step lengths. A more extended posture may also result in fluctuations of the centre of mass during walking as a result of the swinging-pendulum mode of walking that may actually increase the energetic cost of locomotion.
Polk (2004) also raises an interesting point that fully extended posture is rare among living mammals and bipedal birds, suggesting that this method may not be energetically favourable. There is however, disagreement among researchers on the posture of Neanderthals during walking; there is no real consensus if it were more extended, like modern humans, or more flexed like primates (Polk 2004). Even with the fully articulated skeleton of the Neanderthal achieved it is difficult to confidently determine what posture it would maintain.
What about running?
Homo sapiens are relatively poor runners in comparison to many mammals with a top speed of 10.2 m s-1. Homo, however, are capable of a type of running uncommon in other mammals and not observed in primates; endurance running (Bramble and Lieberman 2004), a fit H. sapien can regularly run 10 Km and practised individuals can run marathon distances of 42 Km. The endurance running hypothesis suggests that endurance running is a selective advantage because hominids run at the same speeds that mammal’s gallop resulting in the animal panting causing them, eventually, to over-heat, allowing for the kill (Carrier 1984).
This type of running may perhaps be an explanation for Homo success. H. sapien running, however, is approximately 50% more energetically expensive than walking and results in a number of stresses on the human skeleton, especially when the heel hits the floor at the start of stance phase.
One strategy to reduce the impact shock from the ground is to increase the joint surfaces to dissipate the forces, this has been found to be true for Homo species, having substantially larger articular surfaces at the femoral-tibial (Knee) joint (Bramble and Lieberman 2004).
Recent research suggests that endurance running efficiency is strongly related to the length of the Achilles tendon, which attaches the gastrocnemius and soleus muscles to the posterior surface of the calcaneus (heel bone) (Raichlen et al. 2011). Running requires spring-like tendons (such as the Achilles) to store energy from the impact in the stance phase to release at the start of the swing phase to ‘kick-off’ during the run, these tendons are estimated to save about 50% of the metabolic cost of running (Alexander 1991).
The shorter the moment arm of the Achilles tendon the greater amount of energy storage possible. The Achilles tendon attaches to the back of the calcaneus (heel) and thus a longer calcaneus correlates with a longer moment arm and a reduced efficiency with running energy (Raichlen 2011).
Researchers have noted that the Neanderthal calcaneus is approximately 8% longer than in H. sapien (Trinkaus 1983), it is therefore safe to assume that the running efficiency of H. sapien would have been better than that of the Neanderthal. This would confer a selective advantage when hunting prey without the use of weapons or projectiles and particularly the hunting of larger mammals (Carrier 1984).
While a longer calcaneus is not correlated with running efficiency, it could have improved activities that require a greater moment such as walking uphill or jumping (Thorpe et al. 1998). The more robust Neanderthal femur may have also produced greater mechanical advantage improving the efficiency of knee extensor and ankle plantar flexor muscles (Trinkaus 1983).
This means that Neanderthals would have been more efficient at jumping and walking over uneven terrain, which is perhaps supported by the presence of ‘squatters facets’ on the Neanderthal tibiae (Figure 7.) (Stringer and Gamble 1993). These facets are a sign of repetitive jumping and squatting, it may also be likely that constant uphill walking may generate these as well. It was also stated earlier that more extended postures require flexion before jumping can occur, reducing reaction speed and manoeuvrability. And, as there is evidence that Neanderthals used spears for hunting, coupled with the fact that Neanderthals are found in relatively colder climates in which the prey animal would likely not overheat from extended galloping (Entin et al. 1998). Leads us to conclude that the skeletal-anatomy of the Neanderthal is highly adapted for manoeuvrability and quick reactions, which would suit their hunting strategy of facing prey directly and may have lead to a significant advantage over humans in a cold and uneven environment.
Figure 7. Anterior surface of the distal tibia showing the presence of ‘squatters facets’ as a result of repetitive squatting and jumping (Singh 1959).
It is clear then, that in a flat and warm environment with identical hunting styles, the superior locomotive efficiency of the H. sapien would give a greater advantage in hunting and energy utilisation, this could have led to the extinction of Neanderthals if they were in direct competition. However, morphological variations between H. sapien and Neanderthal were likely to have been adapted for different activities and it could also be suggested that their locomotion strategy may have been different entirely.
This article has served (I hope) to demonstrate that, against common conceptions, the Neanderthal was a very well developed and adapted species that would have significant advantages in different situations.
This leads us to conclude that the extinction of the Neanderthals was unlikely due to locomotive deficiencies. Some researchers suggest they were already heading to extinction prior to the appearance of the H sapien (Higham 2014) and so climatic conditions or disease may have led to their demise.
While this may have shed some light on the locomotive efficiencies of Neanderthal and H. sapiens however, this should also be analysed in concordance with the upper limb capabilities of Neanderthals and H. sapien, better hand dexterity may have allowed for more food acquisition by foraging as well as hunting.
It is also important to consider this debate in the context of human evolution, with Neanderthal and H. sapien representing just two of the most recent hominid species it would make sense to compare the musculoskeletal anatomy of older hominid species. This would show us if there was an evolutionary trend for extended tibiae or more gracious bone structure, suggesting then that the current human form may be the most energetically efficient and overall better competitor.
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