Locomotor decoupling and the origin of hominin bipedalism
Introduction
Bipedal locomotion is a pivotal development in the course of hominin evolution. Its importance was appreciated early in human evolutionary studies (Dart, 1925; Darwin, 1871) and bipedalism has long been regarded as “the basic adaptation for the foundation of the human radiation starting man on his ‘separate evolutionary path’” (Washburn, 1951, Washburn, 1959; from Hewes, 1961, p. 687). Scientists now recognize that habitual terrestrial bipedalism was the first uniquely hominin attribute to evolve and that it predisposed hominins to evolve other uniquely human traits (Ward, 2002). The question of whether a fossil species is a hominin can be appropriately posed as: was it a biped?
Since Dart's (1925) initial australopithecine discovery, a great deal of research has been dedicated to reconstructing early hominin behaviors. Ward (2002) distinguishes between two separate, although complementary, research questions concerning early hominin locomotion. First, researchers endeavor to reconstruct the daily locomotor behaviors of early hominins and evaluate their relative capacities for different locomotor adaptations. A great deal of study has been dedicated to this end and, although debate persists, the question is ever closer to resolution (Berge, 1991, Berge, 1994; Crompton et al., 1998; Duncan et al., 1994; Jungers, 1988, Jungers, 1991; Kramer, 1999; Kramer and Eck, 2000; Latimer et al., 1987; Latimer and Lovejoy, 1989, Latimer and Lovejoy, 1990a, Latimer and Lovejoy, 1990b; Lovejoy, 1988; Lovejoy et al., 1973; MacLatchy, 1996; Rak, 1991; Spoor et al., 1994; Stern and Susman, 1983, Stern and Susman, 1991; Susman et al., 1984).
The second question is to determine the selective pressure that caused hominin bipedalism to evolve. Numerous selective pressures and corresponding scenarios have been put forth to account for the origin of bipedalism. The proposed selective pressures include: provisioning (Lovejoy, 1981), vigilance (Dart, 1925; Darwin, 1871), terrestrial efficiency (Rodman and McHenry, 1980), transporting food (Hewes, 1961), transporting infants (Sinclair et al., 1986), transporting tools (Washburn, 1960), effective tool use (Marzke, 1986), behavioral displays (Jablonski and Chaplin, 1993), seed eating (Jolly, 1970), increased foraging efficiency (Wrangham, 1980), feeding posture (Hunt, 1994), hylobatian model (Tuttle, 1975, Tuttle, 1981) and thermoregulation (Wheeler, 1991a, Wheeler, 1991b). Despite these diverse hypothesized pressures and the tremendous amount of research, no theory has been met with universal support. Consequently, understanding the origin of bipedalism continues to be an elusive goal for paleoanthropology.
The purpose of this paper is to explore a possible increase in fitness resulting from the relaxation of the selective pressure for shoulder stability, which would have accompanied the adoption of bipedalism. I employ adaptive landscapes and mathematical models of well-established concepts from evolutionary biology and apply them to aspects of primate anatomy and behavior. When synthesized, the adaptive landscapes and models produce a series of visually interpretable results that provide the conceptual underpinning for a testable new hypothesis for the origin of bipedalism called the Decoupling Hypothesis (DH). The DH posits that hominin bipedalism is an adaptation that reduces the selective pressure for shoulder stability so that hominins could simultaneously achieve highly effective terrestrial and suspensory behaviors, a combination not accessible to quadrupeds because of a trade-off in shoulder stability and mobility. Negative affects on fitness related to changes in hind limb morphology are not included in the models, but are discussed.
A review of the numerous forms of primate locomotion reveals that most primates, excluding a few notable exceptions, naturally use both the forelimbs and hind limbs simultaneously (Hunt et al., 1996). Since all four limbs act cooperatively during locomotion, the general primate body plan can be considered to consist of a single “locomotor module,” a term Gatesy and Dial (1996, p. 331) define as “anatomical subregions of the musculoskeletal system that are highly integrated and act as functional units during locomotion.” Humans are similar to other primates in predominantly utilizing a single locomotor module, but have diverged markedly from the quadrupedal pattern. In modern humans, the forelimbs are freed from weight bearing responsibilities, and that entire burden has shifted to the hind limbs. Thus, for primates, quadrupedism represents the primitive state, while bipedalism is the derived one. To understand the origin of hominin bipedalism is to understand the reallocation of weight bearing function during terrestrial locomotor from four limbs to two. Because the forelimb was relieved of its weight bearing function, and the shoulder transmits forces from the forelimb to the body when engaged in locomotion, the shoulder may prove a fruitful place to search for evidence of the selective pressure that caused bipedalism. To begin, pertinent evolutionary concepts and aspects of primate biology will be examined.
Section snippets
Adaptive landscapes
The phenotypic adaptive landscape, a descendent of Wright's (1932) adaptive landscapes relating fitness to genotypes, was originally described by Simpson (1944) as an approach to bridge the conceptual gap between micro- and macroevolutionary processes (Arnold et al., 2001). Simpson (1944) used landscapes to illustrate several critical concepts in evolution, including: phenotypic variation, selection, response to a changing environment, speciation, and adaptive radiation (Arnold et al., 2001).
Ecological niches, locomotor behaviors and demands on primate shoulders
Primates are characterized by a number of specialized features that are related to life in an arboreal habitat, including a relatively mobile shoulder necessary to navigate discontinuous canopy supports (Clark, 1959). The importance of mobility is evident in primate shoulder morphology which is typified, relative to non-primates, by a globular, highly curved humeral head and a small, relatively flat glenoid fossa (Larson, 1993). While generally more mobile than other mammals, primate shoulders
Trade-off constraints and primate shoulders
While the demands for stability and mobility are independent and the combinations virtually limitless, the actual morphology that a primate shoulder can physically attain is constrained because of a trade-off (negative correlation) between joint stability and mobility. A trade-off is “an inescapable compromise between one trait and another” that makes it “impossible for any population of organisms to evolve optimal solutions to all agents of selection at once” (Freeman and Herron, 1998, p. 297
Key innovations and evolutionary decouplings
Accelerations in the rate of evolutionary change of characteristics of an organism are usually called “Key Innovations,” especially when they are triggers for diversification (Galis, 2001). Most definitions of key innovations suggest that they increase the number of independent traits and potential versatility of the body plan, opening new character space and allowing for the occupation of more niches (Galis, 2001). Hominin bipedalism appears to be such a key innovation. Four types of key
Methods
Adaptive landscapes were modeled in the statistical package R (R Development Core Team, 2005) as a bivariate cumulative normal distribution using the pmvnorm function. The x-, y- and z-axes represent the stability and mobility of the shoulder and the shoulder fitness of that combination (or phenotype), respectively. Each varies from zero to one. For the shoulder traits, zero is no capacity and one is maximal capacity for that trait. The shoulder fitness of a phenotype is the cumulative
Results
Fig. 4 depicts the maximum possible fitness for the 900 theoretical niches. The two horizontal axes represent the demands for mobility and stability, and the vertical axis represents the maximum possible fitness along the line of attainable shoulder morphologies. The effect of the trade-off constraint on primate fitness is that there is a large area of the graph, representing many potential niches, where the maximum possible fitness approaches zero. These represent niches that have intense
Discussion
The results in Fig. 4 show that there are many niches (those that require highly stable and highly mobile shoulders) in which the maximum fitness of any attainable morphology is very low, approaching zero. Thus, niches that require highly effective forms of terrestrial (or above-branch) quadrupedism and suspensory behaviors are unavailable to quadrupedal primates. Many factors probably influence how effective a primate needs to be at locomotor and postural behaviors. Factors affecting
Conclusion
The results presented here offer paleoanthropology a new testable hypothesis for the origin of hominin bipedalism. The DH posits that bipedalism is the result of a selective pressure that increased the independence of the forelimb and the hind limbs with respect to locomotor function. Bipedalism would have allowed early hominin to occupy niches that mandated highly effective terrestrial and suspensory behaviors which would not have been available to quadrupeds because of the trade-off between
Acknowledgments
I would like to express my gratitude to Dr. Patricia Kramer for many helpful discussions about the concepts in, and critical evaluations of, this paper. I thank Dr. Lyle Konigsberg for patient instruction in R and for reviews. I thank Dr. Kevin Hunt for reviews of earlier incarnations as well as Dr. Andrea Taylor. I thank Dr. Andrew Kramer for comments, criticisms and guidance during the development of this work. I am also greatly indebted to Dr. Angi Christensen for countless reviews and
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