Dennis M. Bramble

Endurance running and the evolution of Homo

Striding bipedalism is a key derived behaviour of hominids that possibly originated soon after the divergence of the chimpanzee and human lineages. Although bipedal gaits include walking and running, running is generally considered to have played no major role in human evolution because humans, like apes, are poor sprinters compared to most quadrupeds. Here we assess how well humans perform at sustained long-distance running, and review the physiological and anatomical bases of endurance running capabilities in humans and other mammals. Judged by several criteria, humans perform remarkably well at endurance running, thanks to a diverse array of features, many of which leave traces in the skeleton. The fossil evidence of these features suggests that endurance running is a derived capability of the genus Homo, originating about 2 million years ago, and may have been instrumental in the evolution of the human body form.

The human gluteus maximus and its role in running

SUMMARY The human gluteus maximus is a distinctive muscle in terms of size, anatomy and function compared to apes and other non-human primates. Here we employ electromyographic and kinematic analyses of human subjects to test the hypothesis that the human gluteus maximus plays a more important role in running than walking. The results indicate that the gluteus maximus is mostly quiescent with low levels of activity during level and uphill walking, but increases substantially in activity and alters its timing with respect to speed during running. The major functions of the gluteus maximus during running are to control flexion of the trunk on the stance-side and to decelerate the swing leg; contractions of the stance-side gluteus maximus may also help to control flexion of the hip and to extend the thigh. Evidence for when the gluteus maximus became enlarged in human evolution is equivocal, but the muscles minimal functional role during walking supports the hypothesis that enlargement of the gluteus maximus was likely important in the evolution of hominid running capabilities.

The foot core system: a new paradigm for understanding intrinsic foot muscle function

The foot is a complex structure with many articulations and multiple degrees of freedom that play an important role in static posture and dynamic activities. The evolutionary development of the arch of the foot was coincident with the greater demands placed on the foot as humans began to run. The movement and stability of the arch is controlled by intrinsic and extrinsic muscles. However, the intrinsic muscles are largely ignored by clinicians and researchers. As such, these muscles are seldom addressed in rehabilitation programmes. Interventions for foot-related problems are more often directed at externally supporting the foot rather than training these muscles to function as they are designed. In this paper, we propose a novel paradigm for understanding the function of the foot. We begin with an overview of the evolution of the human foot with a focus on the development of the arch. This is followed by a description of the foot intrinsic muscles and their relationship to the extrinsic muscles. We draw the parallels between the small muscles of the trunk region that make up the lumbopelvic core and the intrinsic foot muscles, introducing the concept of the foot core. We then integrate the concept of the foot core into the assessment and treatment of the foot. Finally, we call for an increased awareness of the importance of the foot core stability to normal foot and lower extremity function.

The evolution of marathon running : capabilities in humans.

Humans have exceptional capabilities to run long distances in hot, arid conditions. These abilities, unique among primates and rare among mammals, derive from a suite of specialised features that permit running humans to store and release energy effectively in the lower limb, help keep the body’s center of mass stable and overcome the thermoregulatory challenges of long distance running. Human endurance running performance capabilities compare favourably with those of other mammals and probably emerged sometime around 2 million years ago in order to help meat-eating hominids compete with other carnivores.

Brains, Brawn, and the Evolution of Human Endurance Running Capabilities

Theories about hominin evolution are often connected intimately with notions of what it is to be human. Such ideas have had a particularly strong infl uence on thinking about the defi nition and origin of the human genus (see Landau, 1993; Wood and Collard, 1999; Wood, 2009). Many, if not most scenarios for the evolution of the genus Homo emphasize the importance of quintessentially human traits such as large brains, tool-making, and complex cognition. Usually these derived features have been interpreted, explicitly or implicitly, as a suite of novel strategies that emphasize cognitive over athletic means of competing with the rest of nature (“red in tooth and claw”). Most animals compete with each other to a signifi cant extent using athletic capabilities such as strength, power, agility and speed. Obviously, humans compare poorly with other mammals, including African apes, in these characteristics: we are weak, slow, and awkward creatures. Even though male chimpanzees weigh less than a typical adult modern human, they can produce much more force, can sprint more rapidly, and are obviously more agile during locomotion (Stedman et al., 2004). Yet, although no human alive could match a chimpanzee in hand-to-hand combat, our cognitive capacities are extraordinarily better developed. Accordingly, it seems reasonable to focus on evolutionary scenarios for the genus Homo that explain the triumph of brains over brawn. Interestingly, the idea that humans are poor athletes is demonstrably wrong in one crucial respect. While humans have comparatively poor performance capabilities in terms of power and strength, we are unusually specialized endurance athletes, with surprisingly impressive aerobic performance capabilities. These capabilities are particularly remarkable for endurance running (ER), defi ned as running long-distances (>5 km) using aerobic metabolism. These capabilities, which have been reviewed in depth by Carrier (1984) and Bramble and Lieberman (2004), compare extremely well to other mammals, especially primates, in terms of several performance criteria such as speed and distance, especially in hot conditions.

Impact Loading and Locomotor-Respiratory Coordination Significantly Influence Breathing Dynamics in Running Humans

Locomotor-respiratory coupling (LRC), phase-locking between breathing and stepping rhythms, occurs in many vertebrates. When quadrupedal mammals gallop, 1∶1 stride per breath coupling is necessitated by pronounced mechanical interactions between locomotion and ventilation. Humans show more flexibility in breathing patterns during locomotion, using LRC ratios of 2∶1, 2.5∶1, 3∶1, or 4∶1 and sometimes no coupling. Previous studies provide conflicting evidence on the mechanical significance of LRC in running humans. Some studies suggest LRC improves breathing efficiency, but others suggest LRC is mechanically insignificant because ‘step-driven flows’ (ventilatory flows attributable to step-induced forces) contribute a negligible fraction of tidal volume. Yet, although step-driven flows are brief, they cause large fluctuations in ventilatory flow. Here we test the hypothesis that running humans use LRC to minimize antagonistic effects of step-driven flows on breathing. We measured locomotor-ventilatory dynamics in 14 subjects running at a self-selected speed (2.6±0.1 ms−1) and compared breathing dynamics in their naturally ‘preferred’ and ‘avoided’ entrainment patterns. Step-driven flows occurred at 1-2X step frequency with peak magnitudes of 0.97±0.45 Ls−1 (mean ±S.D). Step-driven flows varied depending on ventilatory state (high versus low lung volume), suggesting state-dependent changes in compliance and damping of thoraco-abdominal tissues. Subjects naturally preferred LRC patterns that minimized antagonistic interactions and aligned ventilatory transitions with assistive phases of the step. Ventilatory transitions initiated in ‘preferred’ phases within the step cycle occurred 2x faster than those in ‘avoided’ phases. We hypothesize that humans coordinate breathing and locomotion to minimize antagonistic loading of respiratory muscles, reduce work of breathing and minimize rate of fatigue. Future work could address the potential consequences of locomotor-ventilatory interactions for elite endurance athletes and individuals who are overweight or obese, populations in which respiratory muscle fatigue can be limiting.

Functional, Developmental and Morphological Integration: The Case of the Head and Forelimb in Bipedal Hominins

Understanding how growing bones adapt to mechanical loading is a fundamental problem in human biology. Exercise-induced changes in bone strength are greater in women who start exercising premenarchally vs. postmenarchally, suggesting that estrogen (E2) may mediate these bone-strain interactions. Here we evaluate the contributions of peripubertal physical activity and estrogen levels to young adult bone strength in subjects from the Penn State Young Women’s Health Study (N=84). We hypothesize that women who 1) had higher E2 levels or 2) were more physically active during puberty will have greater adult bone strength. To test this hypothesis, we divided subjects into tertiles of physical activity and of E2 level. We then compared cross-sectional moment of inertia (CSMI) and section modulus (Z) in the femoral narrow neck, intertrochanteric region, and proximal shaft at age 17 (measured using DXA and the HAS algorithm) among these E2 and activity tertiles. Results indicate that women with the highest E2 levels in the first year after menarche had 11% greater CSMI in the narrow neck and 6-12% greater Z in the narrow neck and intertrochanteric region, vs. women with lower postmenarchal E2 levels. The most physically active women had 16-18% greater femoral CSMI in the narrow neck and intertrochanteric region, and 9-11% greater Z in the narrow neck, vs. less active women. These results support the hypothesis that peripubertal estrogen and physical activity are important determinants of adult bone strength. Physiological factors such as hormone levels may be crucial mediators of human osteogenic responses to exercise.

Head Roll Stabilization and Muscle Mitigation Mechanism in Human Distance Running

Understanding how growing bones adapt to mechanical loading is a fundamental problem in human biology. Exercise-induced changes in bone strength are greater in women who start exercising premenarchally vs. postmenarchally, suggesting that estrogen (E2) may mediate these bone-strain interactions. Here we evaluate the contributions of peripubertal physical activity and estrogen levels to young adult bone strength in subjects from the Penn State Young Women’s Health Study (N=84). We hypothesize that women who 1) had higher E2 levels or 2) were more physically active during puberty will have greater adult bone strength. To test this hypothesis, we divided subjects into tertiles of physical activity and of E2 level. We then compared cross-sectional moment of inertia (CSMI) and section modulus (Z) in the femoral narrow neck, intertrochanteric region, and proximal shaft at age 17 (measured using DXA and the HAS algorithm) among these E2 and activity tertiles. Results indicate that women with the highest E2 levels in the first year after menarche had 11% greater CSMI in the narrow neck and 6-12% greater Z in the narrow neck and intertrochanteric region, vs. women with lower postmenarchal E2 levels. The most physically active women had 16-18% greater femoral CSMI in the narrow neck and intertrochanteric region, and 9-11% greater Z in the narrow neck, vs. less active women. These results support the hypothesis that peripubertal estrogen and physical activity are important determinants of adult bone strength. Physiological factors such as hormone levels may be crucial mediators of human osteogenic responses to exercise.