Daniel E. Lieberman, Ph.D. - US grants

Despite decades of research on locomotor energetics, the role of leg length in determining locomotor energy efficiency and speed remains unclear. This project will investigate the effect of leg length on energy cost and speed during walking and running in human and domestic dogs in order to test a new biomechanical model that incorporates leg length as a determinant of these performance variables. Energy expenditure will be measured at a range of walking and running speeds for both species during treadmill trials. A set of outdoor trials will also be conducted in order to test the effect of leg length on maximum running speed and acceleration, and to investigate tradeoffs between energetic efficiency and maximum speed and acceleration. Results will be used to test predictions of the model, specifically that increased leg length improves energy efficiency and speed during walking and running, but at the cost of decreased acceleration and increased energy necessary to swing the leg. The inclusion of both bipeds (humans) and quadrupeds (dogs) will further provide a means of investigating the link between leg length and locomotor performance across a range of anatomical design. If successful, the model will provide a new method of quantitatively assessing locomotor performance in both living and fossil species by providing a new, potentially more accurate and reliable means of making inferences about locomotor behavior and evolution. As the evolution of the genus Homo is marked by a significant increase in leg length, this model will be especially useful in testing current hypotheses regarding the evolution of hominid locomotor and foraging behavior.

Given the diversity of locomotor adaptations evident in living and extinct species, the inability to predict locomotor performance reliably and quantitatively from limb design represents a significant shortcoming in our understanding of locomotor adaptation and ecology. This study will address this issue by testing a relatively simple model that explicitly incorporates leg length as a determinant of locomotor energy cost, and by testing the effect of leg length on maximum and preferred speeds. This project also will promote the integration of graduate training and research in physical anthropology with experimental physiology and biomechanics.

This study tests a hypothesized mechanism for two well-documented trends in human skeletal evolution: that recent humans are less robust than earlier modern humans, and that humans from warm climates have longer, less robust limbs than humans from cold climates. The general hypothesis is that there is a relationship between limb proportions and skeletal robusticity, because the processes by which bones grow in length and in thickness are both influenced by the hormone estrogen during skeletal growth.

The specific prediction is that variation in estrogen levels among individuals alters 1) the expression of the estrogen receptor, which affects how bones respond to mechanical loading (e.g. from exercise), and 2) the activity of cartilage cells in the growth plate, which affects how bones grow in length. If the extent to which bones respond to mechanical loading varies among individuals or populations, then patterns of human skeletal robusticity may reflect both loading history and changes in the levels of hormones such as estrogen. Similarly, if interactions between estrogen levels and mechanical loading affect bone length, then patterns of limb length may reflect habitual activity as well as adaptations to climate. Distinguishing among these alternatives is crucial for improving our interpretations of human adaptation and behavior.

The 45-day experiment will use 24 sheep (Ovis aries), divided into low, normal and high estrogen treatment groups. Half of each group will be sedentary, and half will exercise daily. Fluorochrome dyes will label bone growth. Real-time reverse transcriptase polymerase chain reaction (rtPCR) will quantitatively measure estrogen receptor-a expression. Proliferating cell nuclear antigen (PCNA) immunoreactivity will measure cartilage cell proliferation. The preliminary experimental results support the hypothesis that variation in estrogen level influences epiphyseal growth and diaphyseal responses to loading, and thus may affect patterns of skeletal robusticity in humans. In a small sample of juvenile sheep, differences in estrogen level and exercise had significant and dramatic effects on periosteal growth rate in the femur and tibia. For example, mean daily apposition rate in the femora of exercised animals is 44% higher in high-estrogen than in low-estrogen animals (p<.05), and 26% higher than in sedentary, high-estrogen animals (p<.05). Epiphyseal height also varies with estrogen level and exercise: the height of the metatarsal growth plate is 41% greater (p<.025), and there are 29% more proliferative chondrocytes (p<.05), in high-estrogen exercised vs. sedentary animals, and the height of the distal tibia growth plate is 25% greater in low-estrogen exercised vs. sedentary animals (p<.025).

This project will promote the integration of graduate training and research in physical anthropology with experimental physiology and skeletal endocrinology. The experiments will address a number of basic biological questions about how interactions between estrogen and strain affect longitudinal and periosteal bone growth. The specific effects of interactions between hormone levels and environmental stimuli on human bone growth have never been studied, but are quite relevant to a number of clinical issues, including the attainment of peak bone density and prevention of osteoporosis. For this reason, the results of this study will be disseminated in biomedical as well as anthropological journals.

It has recently been hypothesized that many novel aspects of human anatomy reflect adaptations for endurance running. But humans, as bipeds, have special problems counteracting the tendency of the head to pitch forward during running, especially when the heel strikes the ground (heelstrike). The hypothesis tested here is that humans have evolved a novel mechanism, partially convergent with that of quadrupedal running animals, for counteracting the tendency of the head to pitch during bouncy running gaits at moderate, endurance speeds. Therefore, the project will study how humans stabilize the head during walking and running, and compare some of these mechanisms with a quadrupedal mammal.
The key component of this project is a biomechanical and anatomical model that incorporates differences between the pendular and mass-spring mechanics of walking versus running. Although humans have vertically-oriented necks with restricted ranges of head movement, the muscular connections between the head and the shoulder are mostly de-coupled in humans, with the primary exception of the a small portion of the trapezius muscle (the cliedocranial trapezius, CCT). Humans also have a nuchal ligament, a tendon-like structure absent in great apes but present in other mammals. The human nuchal ligament connects with the CCT and inserts on the back of the head. Thus when the CCT contracts, it is hypothesized to link the mass of the arm with the mass of the head. Specifically, as the arm and shoulder girdle fall at heelstrike, inertial forces of the arm may passively extend the head just when it tends to pitch forward.
Hypotheses derived from the model will be tested experimentally in humans and sheep during walking and running on a treadmill and force plate at a variety of speeds and with different tasks while looking at a focal point. Various sensors will be used to collect data on positions, accelerations and displacements of the head, shoulder and arms. In addition, electromyography (EMG) data will be obtained from the major muscles involved in head extension.
In terms of scientific merit, the results of these experiments will help improve our understanding of the how humans stabilize their heads during running, a poorly studied subject. While there has been much research on the functional morphology of walking, less is known about running. The results are especially relevant to framing and testing the hypothesis that endurance running played a key role in human evolution.
In terms of broader impact, the experiments planned here will be published in anthropology and biology journals, helping to integrate experimental and evolutionary research in these related fields, and on the web via the Peabody Museum as part of a new exhibit on human evolution. The experiments will provide research opportunities and training for students, as well as for a post-doctoral position. The results will also be useful to the wider audience of people interested in running.

The hands and feet of haplorhine primates (apes and monkeys) have similar intrinsic proportions that tend to correlate with their habitat and mode of locomotion. For example, arboreal quadrupeds (e.g. New World monkeys) have hands and feet with long digits in relation to the palm or sole, and a relatively long first digit enabling a secure grasp on small arboreal supports. Suspensory primates such as gibbons hang below arboreal supports by combinations of forelimbs and hindlimbs, and their extremities have long, curved phalanges. Among terrestrial species, digitigrade quadrupeds (e.g. papionins) have short straight phalanges relative to the metapodials (metacarpals and metatarsals). Remarkably, even humans have similarly proportioned extremities, despite the fact that their hands and feet perform different functions. Human hands and feet are short in relation to the limbs, with short, robust metapodials, short lateral phalanges and a proportionately longer first digit (great toe and thumb). NSF support will allow Campbell Rolian to test whether these skeletal similarities between hands and feet in haplorhines are the result of selection for similar functions, or whether underlying developmental phenomena such as pleiotropy (when one gene locus affects multiple aspects of the phenotype) cause hand and foot bones to be more strongly correlated with each other than with other parts of the skeleton.
Pleiotropic effects between hand and foot developmental genetic programs can have potentially conflicting roles in the evolution of digit morphology. When hand and foot digits evolve to perform similar locomotor functions, pleiotropy should facilitate correlated changes in morphology. However, when hand and foot digits evolve to perform separate functions, then pleiotropic effects may constrain the independent evolution of digital shape in the hands and feet. Campbell will collect morphometric data from the bones of the hands and feet of over 500 individuals from 13 taxa, selected to represent the diversity of locomotor behaviors and breadth of evolutionary relatedness among haplorhines. These data will be used to compare patterns of phenotypic covariation within and between species, testing hypotheses about the importance of function vs development in driving the independent evolution of digit morphology in primates.
Significance and Broader Impacts: Few studies have addressed empirically how developmental constraints may bias natural selection for morphological divergence. Campbell will address this important question by looking at covariation in haplorhine hands and feet. Using primate limb skeletons as a case study, this project will provide broader insight into the patterns and processes of vertebrate morphological evolution, particularly as they relate to the growing field of evolutionary developmental biology (evo-devo). This project also has important implications for the study of human evolution. For instance, results may provide evidence that human hands and feet did not evolve their intrinsic proportions independently. Such information will be critical for testing long-standing hypotheses about the selective history of manipulative ability and bipedalism in the hominin lineage. Additional broader impacts of the study include providing teaching tools for undergraduate education, and the creation of a valuable digital archive of primate hand and foot skeletons. Through publications in peer reviewed journals and presentations at interdisciplinary conferences, this project will also help integrate graduate training and research in physical anthropology with evolutionary developmental biology.

Processing food is a universal human behavior. The effects of food modification on hominin biology are poorly understood, however, and most research focuses on thermal processing (cooking), leaving non-thermal, mechanical processing methods largely unstudied. To address these gaps in understanding, this research tests the effects of simple mechanical processing (pounding and slicing) and cooking (roasting) on masticatory (chewing) performance. The general hypothesis tested is that the effects of mechanical processing on food material properties may help account for dental size reductions within the genus Homo prior to the adoption of cooking. To test this hypothesis, 14 subjects will chew size-standardized samples of raw or processed food. EMG (electromyographic) recordings of muscle activity and correlated bite-force data will be collected from masticatory muscles and a predictive model used to determine whether mechanical processing can account for tooth size decreases prior to the Middle Paleolithic, when archeological evidence for cooking first becomes abundant. The efficiency of food breakdown in the mouth (rate of food fragmentation per chew) and data on the foods' mechanical properties will also be collected.

Intellectual merits- This study is among the first to assess how cooking and mechanical processing of representative foods affect key biomechanical properties of mastication such as chew number, force production and food fragmentation efficiency. There has been much debate concerning cooking in human evolution, but while this study experimentally tests the masticatory performance effects on roasted foods, it also tests other potentially important forms of food processing that probably predate cooking, notably mechanical tenderization and slicing. Broader Impacts- This research promotes graduate education and will result in a Ph.D. for a female graduate student. Additionally, the data generated will increase knowledge on hominin diets, food mechanical properties, processing effects and chewing performance. Given interest in cooking and other food processing techniques, the results are relevant to a wide variety of fields including anthropology, food science, evolutionary biology and anatomy.

This project studies how changes in the body that occurred during human evolution affect the ability to throw well. Humans are unique among primates in being able to throw objects with both great precision and speed. This ability may have helped our ancestors hunt and defend themselves. To better understand the evolution and biomechanical bases for human throwing capabilities, this study investigates how changes in the shape of the bones in the arms, shoulders and back affect throwing performance. The researchers are collecting data on how the body moves during a throw using a high speed, 3D camera system. They will then use a custom written computer program to break down and examine the individual motions of each body part during that throw. These data will be collected from a large sample of individuals who vary in the anatomy of their arms, shoulders and back. In addition, restrictive braces will be used to alter the throwing motion in controlled ways. These manipulations will allow us to assess how different components of the trunk and arms contribute to speed and accuracy.

This project uses an interdisciplinary approach combining aspects of anthropology, biology, physics and sports medicine to address how different aspects of human anatomy relate to throwing performance. A better understanding of this relationship will improve not only our understanding of human evolution, but will also contribute to our knowledge of how injury occurs in throwing athletes.