David R. Carrier

The Energetic Paradox of Human Running and Hominid Evolution [and Comments and Reply]

The energetic cost of running is relatively high in man. In spite of this, humans are adept endurance runners, capable of running down, for example, zebra and kangaroo. Distance running is made possible for man in part by an exceptional ability to dissipate exercise heat loads. Most mammals lose heat by panting, which is coupled to breathing and locomotor cycles during running. This interdependence may limit the effectiveness of panting as a means of heat dissipation. Because sweating is not dependent on respiration, it may be more compatible with running as a thermoregulatory mechanism. Furthermore, mans lack of body hair improves thermal conductance while running, as it facilitates convection at the skin surface. While horses, for example, have been shown to possess energetically optimal speeds in each gait, the energetic cost for a man to run a given distance does not change with speed. It is hypothesized that this is because bipedality allows breathing frequency to vary relative to stride frequency. Mans constant cost of transport may enable human hunters to pursue the prey animal at speeds that force it to run inefficiently, thereby expediting its eventual fatigue. Given what is known of heat dissipation in Old World Anthropoidea, the bipedality of early hominids, and human exercise physiology, one factor important in the origin of the Hominidae may have been the occupation of a new niche as a diurnal endurance predator.

Ontogenetic Limits on Locomotor Performance

For most vertebrates, locomotor activity begins at the time of hatching or birth. Although handicapped by small size, rapidly growing tissues, and naïveté, juveniles of most species must maneuver in the same environment and avoid the same predators as adults. Thus, it is not surprising that some ectothermic and precocial endothermic tetrapods undergo ontogenetic changes that allow juveniles to sprint almost as fast and jump almost as far as adults. Allometric changes that have been shown or suggested to enhance performance in juveniles include relatively longer limbs, relatively greater muscular forces and contractile velocities, and higher muscular mechanical advantage. Compensation for rapid growth has been shown to occur in the bones of precocial birds and mammals. The limb bones of these animals have relatively greater cross-sectional diameters and areas than those of adults. This maintains a parity of bone and muscular strength during periods of rapid growth, when bones are composed of weaker, more flexible tissue. In contrast to their sprinting and jumping performance, young animals appear to have significantly less locomotor stamina and agility than adults. The lower stamina may, in large part, simply be a consequence of juveniles being smaller than their parents. The awkwardness of youth appears to result from a conflict between the process of growth and the effective integration of the sensory, neural control, and motor systems. Because juveniles often suffer higher rates of mortality from predation, selection for improved locomotor performance is likely to be strong. Consequently, as a possible result of ontogenetic canalization, the adult phenotype may be determined as much or more by selection on the locomotor performance of juveniles as by direct selection on the locomotor abilities of adults.

The evolution of locomotor stamina in tetrapods: circumventing a mechanical constraint

Endothermic tetrapods differ dramatically from ectothermic tetrapods in having a great capacity to sustain vigorous locomotion. I suggest that this difference reflects alternative adaptive responses to a mechanical constraint that was an inherent consequence of the vertebrate transition from aquatic to terrestrial modes of locomotion and respiration. The earliest tetrapods may not have been able to walk and breathe at the same time. Their sprawling gait and lateral vertebral bending would have required unilateral contractions of the thoracic musculature that may have interfered with the bilateral movements necessary for breathing. Modern lizards, whose locomotor and respiratory anatomy resembles that of the early tetrapods, provide support for this hypothesis because their breathing is greatly reduced during locomotor activity. Tetrapod lineages that gave rise to modern ectotherms apparently retained the constraint, becoming either highly specialized for burst activity based on anaerobic metabolism or specialized in passive mech- anisms of defense against predators. The lineages from which birds and mammals are derived have undergone morphological changes that enable simultaneous running and breathing. In modern tetrapods upright posture is correlated with endothermic metabolism. This correlation may have arisen to circumvent ancestral constraints on locomotor stamina.

Genetic basis for systems of skeletal quantitative traits: Principal component analysis of the canid skeleton

Evolution of mammalian skeletal structure can be rapid and the changes profound, as illustrated by the morphological diversity of the domestic dog. Here we use principal component analysis of skeletal variation in a population of Portuguese Water Dogs to reveal systems of traits defining skeletal structures. This analysis classifies phenotypic variation into independent components that can be used to dissect genetic networks regulating complex biological systems. We show that unlinked quantitative trait loci associated with these principal components individually promote both correlations within structures (e.g., within the skull or among the limb bones) and inverse correlations between structures (e.g., skull vs. limb bones). These quantitative trait loci are consistent with regulatory genes that inhibit growth of some bones while enhancing growth of others. These systems of traits could explain the skeletal differences between divergent breeds such as Greyhounds and Pit Bulls, and even some of the skeletal transformations that characterize the evolution of hominids.

Evidence for Endothermic Ancestors of Crocodiles at the Stem of Archosaur Evolution

Physiological, anatomical, and developmental features of the crocodilian heart support the paleontological evidence that the ancestors of living crocodilians were active and endothermic, but the lineage reverted to ectothermy when it invaded the aquatic, ambush predator niche. In endotherms, there is a functional nexus between high metabolic rates, high blood flow rates, and complete separation of high systemic blood pressure from low pulmonary blood pressure in a four‐chambered heart. Ectotherms generally lack all of these characteristics, but crocodilians retain a four‐chambered heart. However, crocodilians have a neurally controlled, pulmonary bypass shunt that is functional in diving. Shunting occurs outside of the heart and involves the left aortic arch that originates from the right ventricle, the foramen of Panizza between the left and right aortic arches, and the cog‐tooth valve at the base of the pulmonary artery. Developmental studies show that all of these uniquely crocodilian features are secondarily derived, indicating a shift from the complete separation of blood flow of endotherms to the controlled shunting of ectotherms. We present other evidence for endothermy in stem archosaurs and suggest that some dinosaurs may have inherited the trait.

Ground forces applied by galloping dogs

SUMMARY The gallop differs from most other quadrupedal gaits in that each limb plays a unique role. This study compares the ground forces applied by the four limbs and uses force differences between limbs to address the question of why the gallop is the fastest quadrupedal gait. Individual ground forces were recorded from each of the four limbs as six dogs galloped down a runway at constant speed. Trials were videotaped at high speed using a camera positioned perpendicular to the runway, and velocity was measured using photosensors. The trailing forelimb applied greater peak vertical forces than the lead forelimb, however the vertical impulses from the two forelimbs were similar because the lead forelimb had a longer contact interval. The trailing forelimb and lead hindlimb applied greater peak accelerating forces and accelerating force impulses than their contralateral limbs despite their tendency to have shorter contact intervals. The accelerating impulse of both forelimbs combined did not differ significantly from that of both hindlimbs. The forelimbs applied a greater decelerating impulse than the hindlimbs, such that their net fore-aft impulse was decelerating whereas that of the hindlimbs was accelerating. The greater accelerating impulse applied by the trailing forelimb and greater decelerating impulse applied by the lead forelimb are consistent with the forelimbs acting as elastic struts rather than being actively retracted. In contrast, greater accelerating forces were produced by the lead hindlimb while the center of mass was lifted, suggesting that the hindlimbs are more actively extended or retracted during stance. The differences in ground forces measured between paired limbs suggest that the lead forelimb and trailing hindlimb are limited in their ability to apply forces by their positions in the stride cycle rather than by their muscular capacity. Although a bound or half-bound would allow more limbs to produce their maximal forces, a gallop may generate higher speeds because it is more efficient. Galloping could be more efficient than other gaits involving sagittal bending if the increased number of ground contact intervals decreased either the decelerating forces applied at the onset of ground contact or the vertical motion of the center of mass.

Effects of mass distribution on the mechanics of level trotting in dogs

SUMMARY The antero–posterior mass distribution of quadrupeds varies substantially amongst species, yet the functional implications of this design characteristic remain poorly understood. During trotting, the forelimb exerts a net braking force while the hindlimb exerts a net propulsive force. Steady speed locomotion requires that braking and propulsion of the stance limbs be equal in magnitude. We predicted that changes in body mass distribution would alter individual limb braking–propulsive force patterns and we tested this hypothesis by adding 10% body mass near the center of mass, at the pectoral girdle, or at the pelvic girdle of trotting dogs. Two force platforms in series recorded fore- and hindlimb ground reaction forces independently. Vertical and fore–aft impulses were calculated by integrating individual force–time curves and Fourier analysis was used to quantify the braking–propulsive (b–p) bias of the fore–aft force curve. We predicted that experimental manipulation of antero–posterior mass distribution would (1) change the fore–hind distribution of vertical impulse when the limb girdles are loaded, (2) decrease the b–p bias of the experimentally loaded limb and (3) increase relative contact time of the experimentally loaded limb, while (4) the individual limb mean fore–aft forces (normalized to body weight + added weight) would be unaffected. All four of these results were observed when mass was added at the pelvic girdle, but only 1, 3 and 4 were observed when mass was added at the pectoral girdle. We propose that the observed relationship between antero–posterior mass distribution and individual limb function may be broadly applicable to quadrupeds with different body types. In addition to the predicted results, our data show that the mechanical effects of adding mass to the trunk are much more complex than would be predicted from mass distribution alone. Effects of trunk moments due to loading were evident when mass was added at the center of mass or at the pelvic girdle. These results suggest a functional link between appendicular and axial mechanics via action of the limbs as levers.

The evolution of pelvic aspiration in archosaurs

Abstract Movements of the pelvic girdle have recently been found to contribute to inspiratory airflow in both crocodilians and birds. Although the mechanisms are quite different in birds and crocodilians, participation of the pelvic girdle in the production of inspiration is rare among vertebrates. This raises the possibility that the pelvic musculoskeletal system may have played a role in the ventilation of basal archosaurs. Judging from the mechanism of pelvic aspiration in crocodilians and the structure of gastralia in basal archosaurs, we suggest that an ischiotruncus muscle pulled the medial aspect of the gastralia caudally, and thereby helped to produce inspiration by increasing the volume of the abdominal cavity. From this basal mechanism, several archosaur lineages appear to have evolved specialized gastralia, pelvic kinesis, and/or pelvic mobility. Kinetic pubes appear to have evolved independently in at least two clades of Crocodylomorpha. This convergence suggests that a diaphragmatic muscle may be basal for Crocodylomorpha. The pelvis of pterosaurs was long, open ventrally, and had prepubic elements that resembled the pubic bones of Recent crocodilians. These characters suggest convergence on the pelvic aspiratory systems of both birds and crocodilians. The derived configuration of the pubis, ischium and gastralia of non-avian theropods appears to have enhanced the basal gastral breathing mechanism. Changes in structure of the pelvic musculoskeletal system that were present in both dromaeosaurs and basal birds may have set the stage for a gradual reduction in the importance of gastral breathing and for the evolution of the pelvic aspiration system of Recent birds. Lastly, the structure of the pelvis of some ornithischians appears to have been permissive of pubic and ischial kinesis. Large platelike prepubic processes evolved three times in Ornithischia. These plates are suggested to have been instrumental in an active expansion of the lateral abdominal wall to produce inspiratory flow. Thus, many of the unique features found in the pelvic girdles of various archosaur groups may be related to the function of lung ventilation rather than to locomotion.

Functional trade-offs in the limb muscles of dogs selected for running vs. fighting

The physical demands of rapid and economical running differ from those of physical fighting such that functional trade‐offs may prevent simultaneous evolution of optimal performance in both behaviours. Here we test three hypotheses of functional trade‐off by measuring determinants of limb musculoskeletal function in two breeds of domestic dogs that have undergone intense artificial selection for running (Greyhound) or fighting performance (Pit Bull). We found that Greyhounds differ from Pit Bulls in having relatively less muscle mass distally in their limbs, weaker muscles in their forelimbs than their hindlimbs, and a much greater capacity for elastic storage in the in‐series tendons of the extensor muscles of their ankle joints. These observations are consistent with the hypothesis that specialization for rapid or economical running can limit fighting performance and vice versa. We suggest that functional trade‐offs that prevent simultaneous evolution of optimal performance in both locomotor and fighting abilities are widespread taxonomically.

The influence of foot posture on the cost of transport in humans

SUMMARY Although humans appear to be specialized for endurance running, the plantigrade posture of our feet, in which the heel contacts the substrate at the beginning of a step, seems incompatible with economical running. In this study, we tested the hypothesis that plantigrade foot posture reduces the energetic cost of transport (COT) during walking in humans. When human subjects walked with their heels slightly elevated in a ‘low-digitigrade’ posture, COT increased by 53% above that of normal plantigrade walking. By contrast, there was no difference in COT when subjects ran with digitigrade versus plantigrade foot posture. Stride frequency increased and stride length decreased when subjects switched to digitigrade walking; however, this change did not influence the COT. Additionally, we found that possible reductions in postural stability appear not to have caused the elevated cost of digitigrade walking. Digitigrade walking, however, did (1) increase the external mechanical work performed by the limbs; (2) reduce the pendular exchange of kinetic and potential energy of the center of mass; (3) increase the average ground reaction force moment at the ankle joint; and (4) increase the recruitment of major extensor muscles of the ankle, knee, hip and back. These observations suggest that plantigrade foot posture improves the economy of walking. Relative to other mammals, humans are economical walkers, but not economical runners. Given the great distances hunter-gatherers travel, it is not surprising that humans retained a foot posture, inherited from our more arboreal great ape ancestors, that facilitates economical walking.