Why did bipedal locomotion emerge amongst terrestrial vertebrates?

Introduction

Bipedality has evolved independently in different lineages among terrestrial vertebrates (Snyder R. C., 1962). In extant mammals, it has evolved independently in primates, kangaroos, and rodents (Wu, et al., 2014) and it has also evolved once in dinosaurs (Sereno P. F., 1993). This essay will therefore be split into three parts. The first will deal with human obligate bipedalism with reference to facultative bipedality in other primates. The second will deal with obligate bipedality in dinosaurs, the origin of which is assumed to be the same for Aves, and will highlight an interesting theory that uses lizard facultative bipedalism as an analogy for early bipedal evolution. Finally, obligate saltatory gait in marsupials and rodents, which had different origins but may have evolved for the same purpose, will be discussed.

Hominin Bipedality

More than 30 hypotheses for hominin obligate bipedalism have been proposed, indicating that many authors are unconvinced by previous theories (Niemitz, 2010). Some of the most prevailing theories include thermoregulation (Wheeler, 1984) and vigilance (Ravey, 1978). The thermoregulation hypothesis suggests that an upright posture was advantageous for reducing the surface area of the body exposed to radiation. The vigilance hypothesis suggests that Miocene hominoids needed an upright posture to spot approaching predators when they moved from forested areas to grassland. Both these hypotheses have been largely out of favour as it became more widely accepted that bipedalism was seen in early hominins that were still arboreal (Clarke & Tobias, 1995). The fossil of the early Australopithecus afarensis A.L. 288-1 (or “Lucy”) skeleton suggests an adaptation for upright posture and bipedal locomotion 3.2 million years ago. This is long before the first tools or a unique brain necessary to make such tools were evident among our ancestors (Lovejoy, 1988). However, that is not to say that A. afarensis were obligate bipeds or exclusively terrestrial. Pan-like features are still evident in the A. afarensis feet alongside adaptations for bipedal locomotion. This intermediary foot between a foot developed for arboreality and one adapted for bipedality suggests Australopithecus may have continued to be arboreal to some extent and possibly was a facultative biped rather than an obligate biped (Clarke & Tobias, 1995). The upper body morphology similarities between Australopithecus and apes, such as a cone-shaped ribcage, further suggest our bipedal ancestors were still adapted for arm-hanging. Our closest living relatives, the chimpanzees, use a bipedal feeding posture both arboreally and terrestrially. This suggests that bipedal behaviour may have originated arboreally rather than terrestrially and more specifically may have originated as a feeding posture (Hunt K., 1996). Some scapulae morphological changes can be observed over the lifetime of an organism depending on the locomotor behaviour. Using this information, the scapulae development of A. afarensis also suggests signs of suspensory behaviour (Green & Alemseged, 2012). Evidence that human wrist morphology indicates a knuckle-walking ancestor has previously been attributed to terrestrial bipedality evolving from terrestrial quadrupedal locomotion (Richmond & Strait, 2000). However, the difference between the extended wrist posture in arboreal knuckle-walkers and the neutral wrist posture in terrestrial knuckle-walkers with the presence of the former in the human wrist further supports an arboreal ancestor (Kivell, Schmitt, & Walker, 2009). Additional support for the adaptive benefit of arboreal bipedalism can be found by observing orangutans, a species of great ape that is still significantly arboreal. Orangutan bipedal behaviour is strongly correlated with both thinner branches and the availability of support branches. Orangutans also respond to these more flexible branches by increasing knee and hip extension, thereby standing more upright (Thorpe, Holder, & Crompton, 2007). Arboreal bipedalism may not have constrained the later development of terrestrial bipedalism. Gibbons are capable of terrestrial bipedal walking at speeds above the threshold which humans have to transition to a running gait. This suggests that there may not be a need for structural specialisations to adopt facultative bipedal locomotion terrestrially (Vereecke, 2006). If postural feeding caused early hominins to exhibit bipedal behaviour initially then what caused habitual bipedalism? Making food piles has been found to motivate chimpanzees and bonobos to elicit bipedal locomotion and creating a platform that requires postural bipedalism to reach food on the platform has been found to elicit postural bipedalism in chimpanzees (Videan, 2002). This supports the hypothesis that bipedalism in hominids could have been motivated by freeing the hands for carrying food (Hewes, 1961) and foraging for elevated food (Hunt K. D., 1994). Wading in shallow waters has also been hypothesised to motivate prolonged bipedal posture and bipedal locomotion. After that, selective factors such as thermoregulation, running and carrying tools may have driven the evolutionary anatomical changes (Niemitz, 2010). However, it may not have been necessary to have significant advantages to bipedalism as similar costs between facultative bipedal and quadrupedal locomotion suggest bipedal locomotion wouldn’t have been a constraint that early hominins would have needed to overcome (Pontzer, Raichlen, & Rodman, 2014).

Bipedality in Dinosaurs

Dinosaurs are thought to have evolved from a single small bipedal ancestor similar to the Eoraptor lunensis (Sereno P. F., 1993). Early dinosaurs had forelimbs that were reduced in size compared to their hindlimbs, with predatory manus with grasping and raking capabilities suggesting predatory behaviour (Sereno P. C., 1994). However, this theory has been questioned as bipedalism for predation is not found in other lines of predators. An opposing theory was proposed based on the hindlimbs and tail as factors that increased the likelihood of bipedalism in the ancestors of dinosaurs. This hypothesis uses the facultative bipedalism seen in some Squamata as they accelerate to suggest a similar development of bipedalism in dinosaurs which both have large caudofemoral muscles in the hindlimbs, outsizing forelimbs in many cases, shifts the bodies centre of mass (BCOM) caudally. It was also suggested that this would explain why so few mammals are bipedal, as synapsids lost the large caudofemoral muscle enhanced hindlimbs sometime during the Late Permian (Persons & Currie, 2017). The elongated hindlimbs of lizards have been found to correlate with stride length and speed. Different species of lizard also have different joint angles during bipedal running. This is interesting as it would indicate the independent evolution of facultative bipedalism among lizards, suggesting bipedalism did not result from the retention of ancestral traits (Irschick & Jayne, 1999). It has been hypothesized that the caudal shift of the BCOM can improve maneuverability as the inertial resistance against rotation is small. This caudal shift may also cause bipedality while accelerating. In fact, some species, such as the Uma scoparia, actively lift their tail to manipulate the BCOM, suggesting there is an advantage to bipedalism (Aerts, Van Damme, D’Août, & Van Hooydonck, 2003). It has been found that the speed for bipedal locomotion was not faster than for quadrupedal locomotion. However, adding to the suggestion that there is some unknown advantage to bipedalism in lizards, some species actively manipulate their BCOM by tucking forelimbs along the side of the body which may allow bipedalism at lower acceleration (Clemente, Withers, Thompson, & Lloyd, 2008).

Bipedalism in Marsupials and Rodents

Saltatory gait has evolved more frequently than alternating bipedal gait in mammals. Most small hopping rodents have a body mass of less than 1 kg except the springhare which is about 4 kg. Extant hopping marsupials, including kangaroos and wallabies, have a body mass from 1 kg to 70kg (Bennett, 2000). It has been suggested that hopping makes traversing irregular terrain easier which is particularly important for rodents and small marsupials. It also may allow rapid deceleration and directional changes (Snyder R. C., 1967). In support of this, when quadrupedal pocket mice were compared with bipedal kangaroo rats, the latter were found to have an advantage over the former when gathering food in open habitats, perhaps because bipedalism acts as an antipredator mechanism (Harris, 1984). Saltatory locomotion in the small kangaroo rats is erratic and thus good for rapid direction and acceleration changes thus supporting the theory that small animals appear to utilise this for predator evasion (Biewener & Blickhan, 1988). Hopping is believed to have evolved in open arid environments for rodents and in more temperate forested environments for marsupials. Resources are patchy and spread widely in both environments. As hopping relates to fast locomotion and is more economical than fast quadrupedal running in some species, both groups of mammals could have benefitted from saltatory behaviour which may have driven the evolutionary changes (Webster & Dawson, 2004). Rodents and small marsupials are below the weight (about 5 kg) at which hopping is thought to become efficient in terms of elastic strain energy storage (Janis, Buttrill, & Figueirido, 2014). However, large saltatory marsupials can store elastic strain energy in muscles and tendons allowing them to save up to 50% of the energy that would otherwise have to be used for locomotion (Baudinette, 1994). Therefore, large saltatory kangaroos and wallabies can hop for long periods of time while small saltatory rodents need to use more muscle work, further supporting the initial benefit of saltatory locomotion in small rodents and marsupials was rapid acceleration for predator avoidance (Moore, Rivera, & Biewener, 2017). Larger saltatory marsupials, which came later and are believed to have evolved from smaller bounding or half-bounding marsupials (Bennett, 2000), may then have been pre-adapted for arid environments.

Conclusion

Obligate bipedality has evolved independently many times. It is not precisely known what caused each instance of bipedality to evolve, however, the adaptive advantages for each independent evolution vary greatly. It is reasonable to believe that hominin bipedalism evolved in our arboreal ancestors as a feeding posture. The adaptations in the upper Australopithecine body strongly suggest that they were arboreal climbers even after the lower body had adapted for bipedalism. Other selective factors such as the carrying hypothesis and the thermoregulation hypothesis may also have been necessary for the development of an upright posture and obligate terrestrial bipedalism. Dinosaurs are believed to have originated from a single bipedal ancestor. One hypothesis for the origin of bipedal behaviour was that the enhanced hindlimbs and tail of the dinosaurs’ ancestors inclined them towards bipedalism. Using facultative bipedalism exhibited among some lizards as an analogy, the caudal shift of the body’s centre of mass in early dinosaurs could have caused bipedality while accelerating. This appears to be advantageous in lizards, some of whom actively shift the body centre of mass caudally to allow bipedal behaviour at lower acceleration. It therefore may have been similarly advantageous among the dinosaurs’ ancestors. Saltatory bipedalism is the most common form of bipedalism among mammals, evolving independently among rodents and marsupials. It was suggested that the origin of saltatory gait, which is good for rapid direction and acceleration changes, evolved for predator evasion and as a method for traversing irregular terrain in small animals. Only later, as the size of some marsupials increased, did it become advantageous for energy saving.

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