Human Evolution and Physical Exercise: The Concept of Being Born to Run

Transcription

1 Human Evolution and Physical Exercise: The Concept of Being Born to Run 1 Livio Luzi 1.1 The Concept of Being Born to Run Born to Run was the third album produced by the American singer-songwriter Bruce Springsteen. It was released by Columbia Records on August 25, The same title was used in the following decades for: at least one novel, an episode in the TV series Terminator, a book on a Mexican tribe of extreme runners, and it even appeared on the cover page of Nature, in November The common denominator of all the uses of Born to Run is the recognition of the need of humans to run in order to survive. 1.2 From Five Billion to One Million Years Ago The present atmosphere of the Earth is composed of 21% oxygen. The remaining gases are nitrogen (78%), argon (0.9%), carbon dioxide and other trace elements (0.012%). About 5 billion years ago, at the birth of our planet, the atmosphere contained virtually no oxygen. The advent of the first forms of life on Earth (prokaryotes, primordial unicellular bacteria) was crucial for the change in composition of the gas content of the atmosphere. Primordial bacteria were able to carry out photosynthesis, utilizing hydrogen, obtained from water, and CO 2 to release oxygen. Therefore the development of life on Earth was determined by the appearance of organisms capable of surviving in the absence of oxygen, with their survival exclusively founded on anaerobic metabolism. The increasing amount of oxygen released by prokaryotes into the primordial atmosphere favored the development of oxidative reactions to produce energy for life, a much more efficient method than anaerobic me- L. Luzi ( ) Department of Sport Sciences, Nutrition and Health University of Milan Milan, Italy livio.luzi@unimi.it L. Luzi (ed.), Cellular Physiology and Metabolism of Physical Exercise Springer-Verlag Italia

2 2 L. Luzi tabolism. Some 1500 million years ago, the first eukaryotes capable of producing energy with oxidative metabolism appeared on Earth. Millions of years were then necessary for the development of multicellular eukaryotes. It is relevant for evolution in general and for human evolution in particular that in parallel with the appearance of more complex multicellular organisms much of the Earth s ecosystem was altered by dramatic geologic events [1]. The volcanic eruptions, continent shifts, and meteoric collisions forced major evolutionary leaps, as only organisms capable of adapting to the new environment survived. One such adaptation is described by the endosymbiotic theory. Endosymbiosis means cohabiting within and in this case refers to the postulated collaboration/interaction between organisms with different metabolic capabilities and dimensions, both of which gain an evolutionary advantage by merging their living environments. As stated, not all organisms were able to tolerate an oxidant atmosphere (i.e., an atmosphere increasingly rich in oxygen produced by photosynthesis). According to endosymbiotic theory, primordial eukaryotes were able to survive due to their incorporation of prokaryotes bearing much-needed complementary skills. Peroxisomes and mitochondria are thought to be remnants of prokaryotes that eventually became eukaryotic organelles, conferring upon their hosts the cellular machinery needed for oxygen detoxification and energy production in aerobiosis [2]. 1.3 The Appearance of the Genus Homo Roughly 1.5 million years ago, Homo erectus appeared on the Earth. Our present genes are similar to those of Homo erectus, Homo habilis, and the first Homo sapiens (200,000 to 100,000 years ago) [3]. Australopithecines were the ancestors of Homo erectus and their evolution was driven by an important change in the ecosystem: the replacement of woodlands by grasslands and savannas in central Africa [4]. The expansion of savannas caused a fundamental change in the way hominids foraged and, consequently, in the quality and caloric content of food as well as the amount of physical activity required to gather food. In fact, the disappearance of woodlands induced hominids to cover longer distances in savannas, prompting the natural selection of individuals with longer lower limbs, the ability to run, better thermoregulatory capacity, and with a higher resting and total daily energy expenditure. Evolutionarily, longer lower limbs and bipedalism facilitated foraging behavior in the new ecosystem, determining a strong association between changes in body size (and metabolism) and ranging/foraging patterns [5, 6]. Therefore, the earliest representative of the human genus, considered to be the African Homo erectus, was indeeed born to run, that is, to cope with an environment strikingly different from the woodlands where previous hominids had gathered food. Several musculoskeletal adaptations are representative of the genus Homo, including a large cranial vault, a prominent nose, a thin mandible, a chin, small teeth, a modified hip joint, and a light skeleton. These anatomic changes allowed our ancestors to walk and run for long distances and times, as their bodies were specialized for endurance and physical activity [7]. Indeed, humans are specifically adapted to engage in prolonged strenuous

3 1 Human Evolution and Physical Exercise: The Concept of Being Born to Run 3 muscular activity, such as efficient long-distance bipedal running. This capacity evolved to allow the running down of game animals by persistent slow but constant chase over many hours. Central to the success of this strategy were at least four distinct factors [8]: (1) energetics: the lower cost of running vs. walking (the other human gait) at speeds above ~2 m/s; (2) skeletal length: as long lower limbs gave Homo erectus greater speed in chasing and hunting; (3) the development of the central nervous system: with the differentiation of specific brain areas responsible for equilibrium, movement coordination, and postural stabilization; (4) thermoregulation: in which the human body, unlike that of animal prey, can effectively remove muscle heat waste. In most animals, a temporary increase in body temperature allows the storage of muscle heat waste. This enables them to escape from animal predators that quickly speed after them for a short duration (the method used by nearly all predators to catch their prey). Unlike other animals that hunt, humans remove body heat with a specialized thermoregulatory system based on sweat evaporation. One gram of sweat can remove 2,598 J of heat energy. Another mechanism is increased skin blood flow during exercise, which allows for greater convective heat loss and is aided by humans upright posture. This skin-based cooling is a function of an increased number of sweat glands combined with a lack of body hair that would otherwise stop air circulation and efficient evaporation. Because humans can remove exercise-generated heat, they can avoid the heat exhaustion that affects animals chased in persistence hunting, and so eventually catch their prey. The amount of food available was much greater in the savannas than in woodlands, mainly due to the higher caloric and protein content of the large herbivores hunted. This produced an increase in the body size of Homo erectus ( 65 kg males and 52 kg females) compared to previous hominids (e.g., Australopithecines, 44 kg males and 31 kg females). The increase in body weight, per se, determined a higher resting energy expenditure (REE: in Homo erectus, an average of 1565 kcal/day in males and 1361 kcal/day in females vs and 902 kcal/day in males and females, respectively, of Australopithecus africanus). By adding the calories consumed by daily activities for Homo erectus to the REE, a total energy expenditure (TEE) of 3165 calories for males and 2141 calories for females can be estimated. These values are quite similar in each case to those of a 70 kg individual contemporary to us [8]. Did Homo habilis actually hunt quadrupeds, or did our earliest ancestors merely scavenge meat from lion and other predator kills? Many experts now believe that Homo habilis scavenged meat from nearby predator kills, chasing away lions with stones and loud calls. The hominids would then grab choice pieces of meat and retreat to a convenient place, far away from predators. There they would eat the fresh meat, and break up the bones for their marrow. Once their hunger was satisfied, they would move off, leaving the crushed bones for other predators to scavenge. The hominids would return to the same place on several occasions. However, their visits were sufficiently infrequent so that carnivores did not hide in wait. Contemporary humans have a genetic background, body size, resting and total energy expenditure comparable to Homo erectus. Nonetheless, the environment of Western countries in which many 21st century humans live has dramatically changed: (1) there is no longer a need to consume energy for food foraging and hunt-

4 4 L. Luzi ing; (2) many more calorie-rich and refined foods are available, in virtually unlimited supply; (3) food deprivation and starvation, except during religious fasts, are unknown (in contrast to the winters and other periods of food scarcity faced by Homo erectus). As a matter of fact, we are currently benefiting from a major ecosystem change that started 10,000 years ago, with the agricultural revolution (when populations of hunters/gatherers settled down and began to raise grains and conserve food for the winter), and reached its apex at the beginning of the 20th century, with the industrial revolution and the introduction of machines to help humans perform laborintensive and energy-demanding tasks. Therefore, due to the mismatch between our genetic background (what we are predisposed for) and our new environment (what we are actually doing), the incidence of diseases such as obesity, type 2 diabetes, metabolic syndrome, hypertension, cardiovascular events, and some forms of cancer has increased dramatically, especially in recent decades [9, 10]. The metabolic mechanism utilized by our body to store rather than to burn calories is insulin resistance. Insulin sensitivity (the opposite of insulin resistance) is defined as the ability of insulin to metabolize a load of glucose (and other energy substrates such as free fatty acids). An impairment of the body s capacity to metabolize a glucose load protects the individual from periods of food scarcity, starvation, or a deficit in carbohydrate or fat intake. Obviously, if evolution selected insulin-resistant humans based on their ability to survive periods of famine, the above-described changes in the 20th century ecosystem have made modern humans susceptible to hyperglycemia, hyperlipidemia, and their pathological consequences, namely diabetes, obesity, and atherosclerotic disease. In principle, more insulin-sensitive individuals should be favored today, as they are able to dispose of regular, high-calorie loads in less time whereas during life on the African savanna they would have been condemned to extinction [9]! The maintenance of normal glycemia is obtained by the balance between insulin secretion and insulin action, a relationship known as glucose tolerance. In normal individuals, there is a hyperbolic relationship between insulin secretion and insulin action (Fig. 1.1); accordingly, normal glucose tolerance can be obtained over a wide range of secretory capacity and insulin action. It is also well established that an imbalance between insulin secretion and insulin action causes hyperglycemia. The secretion of insulin must therefore be considered along with its action in order to determine the metabolic wellness of an individual. It is a common belief that today s marathon runners are the closest modern humans come to Homo erectus in terms of lifestyle and metabolism. Marathon runners maintain a normal glucose tolerance by means of relatively efficient insulin action, tempered by relatively low levels of insulin secretion. In this scenario, hunters/gatherers should have benefited from a very high level of insulin action matched by a low secretory capacity of the hormone. There is an apparent discrepancy between the predisposition of our genes to store energy (the thrifty genotype hypothesis [9] and the highly efficient insulin action of marathon runners (and, probably, of Homo erectus). Thus, an organism predisposed to saving and storing energy needs constant physical exercise to maintain normal insulin action and proper substrate utilization. Accordingly, a healthy lifestyle is defined by regular physical exercise along with appropriate dietary habits. In other

5 1 Human Evolution and Physical Exercise: The Concept of Being Born to Run 5 Fig 1.1 The relationship between insulin sensitivity and beta-cell secretion is well-described by a hyperbolic function, such that the product of insulin sensitivity times beta-cell secretion tends to remain constant. Physical exercise is known to enhance insulin sensitivity. Since less insulin is required to metabolize glucose, a concomitant reduction in beta-cell secretion takes place. The overall effect is as follows: a subject undertaking physical training slides along the hyperbola achieving a position characterized by elevated insulin sensitivity and low circulating insulin levels words, the lack of a physical exercise program renders vain all dietary interventions (this is basically the clinical on the field experience of most physicians). It is worth noting that it is not only the total amount but also the pattern of insulin secretion that determines glucose disposal and the effective clearance a glucose load. First-phase insulin release has been shown to have a consistent role in inhibiting endogenous glucose production following a meal. Early stages of diabetes and obesity are characterized by a loss of first-phase insulin release and thus by postprandial hyperglycemia and a reduction of the thermogenic effect of food. The combination of the two defects leads to diabetes and obesity, respectively (or a combination thereof). Similar to insulin action, the "blindness" of the β-cell to glucose is overcome by amino acid administration via a high-protein diet, indicating that protein homeostasis is the metabolic domain best protected by evolution. In fact, on the one hand, in most conditions (with the notable exception of obesity) insulin s action on protein metabolism is spared (despite a marked impairment of its action on carbohydrate and lipid metabolism). On the other hand, amino acids/high-protein diets are able to restore a normal secretory pattern of insulin secretion, thus overcoming β-cell blindness to glucose during the early stages of type 2 diabetes mellitus. Based on these considerations there are two possibilities. One is that current evolutionary pressure will select one or a few protective genes/features of the sedentary Homo sapiens that will allow humans to evolve such that the insulin sensitivity of future generations is much higher that that conferred by our present genes. In other words, presumably, only individuals with a higher capacity to burn calories and dis-

6 6 L. Luzi pose of nutrient loads (without needing to perform physical exercise) will be selected for survival by evolution. In this case, we have no choice but to passively wait for evolution to find a solution (as our ancestors did!). The other possibility is to change our behavior such that it mimics our ancestors way of life in terms of patterns of physical activity and the diet of hunters/gatherers. That lifestyle was characterized by three cornerstones. First, physical exercise was performed several hours a day, with different modalities and intensities. In Homo erectus, walking and running were frequent forms of physical exercise. The behavior of contemporary species of primates has been studied to deduce the physical exercise patterns and total daily energy expenditure of our ancestors. Although this kind of information is difficult to extrapolate, based on a total energy expenditure of 2,500 3,500 kcal per day, physical exercise, ranging from active to strenuous, was likely performed for between 1 and 4 hours daily. Moreover, even during periods of daily rest and over the year, the average energy expenditure was higher than the present-day value, reflecting non-shivering thermogenesis secondary to cold-temperature exposure. Second, the diet of hunters/gatherers contained a much lower (up to 30% less) percentage of complex carbohydrates than is consumed today, a higher protein content (both vegetable and animal protein), and a total fat content similar to today s level, with the notable prevalence of mono- and polyunsaturated fats over saturated fats. Third, of particular relevance was the modality of caloric intake of Homo erectus, characterized by periods of forced starvation (presumably ranging from 1 day to longer periods). Therefore, periodic fasting was a constant for hunters/gatherers whereas, unless voluntarily performed, periods of food deprivation are for the most part completely unknown in modern Western societies. Interestingly, a metabolic model of fasting is provided by the initial stage of mental anorexia. Patients with this disease voluntarily reduce their caloric intake while engaging in physical exercise for several hours a day. Consequently, body weight, total daily energy expenditure, and blood concentrations of glucose, lipids, and amino acids (with respect to matched controls) are reduced, resulting in a clinical picture that is the mirror image of type 2 diabetes and metabolic syndrome. This clinical model suggests that our genes predispose us with the ability to well resist long periods of reduced caloric intake. If we succeed in changing our lifestyle accordingly, we will eradicate diabetes, obesity, hypertension, metabolic syndrome, cardiovascular disease, and even some forms of cancer. References 1. Kasting JF, Siefert JL (2002) Life and the evolution of Earth s atmosphere. Science 10: Alberts B, Johnson A, Lewis J et al (2002) Molecular biology of the cell. New York, Garland Science 3. Wood B, Collar M (1999) The human genus. Science 284: Cerling TE (1992) Development of grasslands and savannas in East Africa during the neogene. Paleogeog Paleoclimatol Paleoecol 97: Leonard WR, Robertson ML (1997) Comparative primate energetics and hominid evolution.

7 1 Human Evolution and Physical Exercise: The Concept of Being Born to Run 7 Am J Phys Anthropol 102: Ulijaszek SJ (2002) Human eating behaviour in an evolutionary ecological context. Proc Nutr Society 61: Isbell LA, Pruetz JD, Lewis M, Young TP (1998) Locomotor activity differences between sympatric patas monkeys (Erytrocebus Patas) and vervet monkeys (Cercopithecus aethiops): implications for the evolution of long hindlimb length in Homo. Am J Phys Antropol 105: Bramble DL, Lieberman DE (2004) Endurance running and the evolution of Homo. Nature 433: Luzi L, Pizzini G (2004) Born to run: training our genes to cope with ecosystem changes in the twentieth century. Sport Sci Health 1: Neel JV (1962) Diabetes mellitus: a thrifty genotype rendered detrimental by progress. Am J Hum Genetic 14: