energetics

We're pretty much obsessed with the Tour de France here. Today, Gina Kolata writes about the energetic cost of endurance:

By studying four racers as they rode in the 1985 Tour, Klaas Westerterp of Maastricht University in the Netherlands concluded that their metabolic rates increased 4.3- to 5.3-fold. That sort of increase in metabolic rate, he added, is what birds reach when they fly and is thought to be a physiological limit.

David Gordon Wilson, an emeritus professor of mechanical engineering at the Massachusetts Institute of Technology and author of "Bicycling Science" (MIT Press, 2004), calculated that Tour riders generate 400 watts of power when they are riding up mountains or trying to break away from the pack. An average person riding a bicycle and working as hard as possible puts out 150 to 200 watts, he said.

It's the most exciting race for the last several years, with many riders still in contention as they head into the Pyrenées.

Thus says the "Ultramarathon Man," Dean Karnazes, as profiled by Wired (via Instapundit). I think it's fascinating:

If something goes wrong - and it inevitably will - it's usually with Karnazes' feet. In races and on training runs, he has battled giant, foot-devouring blisters. A surprisingly effective treatment: Krazy Glue. Pop the blister, slather the wound with the super-adhesive, and voilà - your foot is ready to take a beating again. The glue acts as a kind of indestructible second skin and has helped Karnazes finish competitions he wouldn't have otherwise. (Officially, Krazy Glue recommends avoiding all contact with skin.)

He devours over 9000 calories a day in his running streaks (a true hunter-gatherer diet of high fat, low sugar, no less), and manages incredible feats:

Over the next 14 years, Karnazes challenged almost every known endurance running limit. He covered 350 miles without sleeping. (It took more than three days.) He ran the first and only marathon to the South Pole (finishing second), and a few months ago, at age 44, he completed 50 marathons in 50 consecutive days, one in each of the 50 states. (The last one was in New York City. After that, he decided to run home to San Francisco.)

I honestly don't understand long distance runners -- I know they exist, but they seem utterly foreign and strange to me. Some think they are the model for ancient humans. As for me, well ...

"Somewhere along the line, we seem to have confused comfort with happiness," he says.

I don't know about you, but I'm not confused!

On the subject of insane feats of endurance, please allow me to draw your attention to this story about extreme children endurance runners:

Marathon children collapse in a copycat race for glory

From Ashling O'Connor in Bombay

A TEN-YEAR-OLD girl from a remote village in eastern India has become the country's latest under-age long-distance runner in a growing craze that has prompted allegations of abuse and exploitation.

Anastasia Barla ran 72 kilometres (45 miles) in the state of Orissa on Monday in sweltering heat before she was forced to stop because of exhaustion.

The girl had been attempting to break the 100km barrier in an effort to outshine Budhia Singh, the four-year-old boy who made world headlines in May when he covered a distance of 65 kilometres in seven hours and two minutes.

Yes, that is not a misprint. A four-year-old boy.

The story mentions other children sent to intensive care after their own attempts on the record.

Now, I know someone will want to make the point that this proves that humans have evolved to be endurance athletes. I will believe that as soon as I find the gland that we evolved to secrete our internal store of high-sugar energy drinks. (I will call it, the Gator-Nipple®). Because without a whole lot of water and sugar, there is no chance that a kid could go more than a few miles.

And then there is this:

Marathon experts maintain that children under 10 should not run more than 15 miles a week.

Well, that's a relief...er, um, fifteen miles a week? May I just say that "marathon experts" are in-sane!

McEwen and Wingfield (2003) discuss the concept of allostasis. I was unfamiliar with this concept myself until an interesting presentation by one of our graduate students the other day. It is distinguished from homeostasis in a way that makes for an interesting contrast that may have relevance to human evolution.

According to the paper (3):

Homeostasis is the stability of physiological systems that maintain life, used here to apply strictly to a limited number of systems such as pH, body temperature, glucose levels, and oxygen tension that are truly essential for life and are therefore maintained within a range optimal for the current life history stage.

Allostasis is achieving stability through change. This is a process that supports homeostasis, i.e., those physiological parameters essential for life defined above, as environments and/or life history stages change. This means that the "set-points" and other boundaries of control must also change. There are primary mediators of allostasis such as, but not confined to, hormones of the hypothalamo-pituitary-adrenal (HPA) axis, catecholamines, and cytokines. Allostasis also clarifies an inherent ambiguity in the term "homeostasis" and distinguishes between the systems that are essential for life ("homeostasis") and those that maintain the systems in balance ("allostasis") as environment and life history stage change.

We note, however, that another view of homeostasis is the operation of coordinated physiological processes that maintain most of the steady states of the organism. In this interpretation, homeostasis and allostasis might seem to mean almost the same thing. The reason they do not is that the notion of "steady state" is itself vague and does not distinguish between those systems essential for life and those that maintain them. It also does not differentiate changes in state to enable reproduction (and other life cycle processes) that are required for immediate survival.

The concept was presented to me in the context of the cost of social competition in primates. Competition--especially reproductive competition--requires that individuals increase their readiness state, their alertness, their rate of vocal communication, and many other behavioral correlates. Ultimately, this relatively excited allostatic state requires an increase in the rate of energy expenditure, mediated by hormonal interactions in the body. Within primate groups, such allostatic states may last for considerable periods of time. One example is the elevated cortisol levels found for male savanna baboons in subordinate ranks. These individuals suffer stress induced by competition from higher-ranked males, resulting in increases in the level of stress hormones, the maintenance of a high level of cardiovascular and mental readiness, and a lack of stress-mediating interactions with other individuals. Together, these behavioral components result in increased energy expenditure, a depression in immune response characterized by an increased rate of opportunistic infections, an increased chance of mortality. Considering the health effects and mortality associated with this allostatic state, we can conclude that the pattern of natural selection acting on energy expenditure and health in baboons would strongly reflect this allostatic state. Other allostatic states probably also have a strong component of selection associated with them, most notably that of the dominant males whose reproductive success depends immediately upon their ability to counter and resist threats from lower ranking males.

McEwen and Wingfield (2003) refer to the excess energetic expenditure associated with an allostatic state as an allostatic load. This represents the cost of maintaining the body in an altered state for a sustained period of time. Allostatic loads may be added to the basic requirements for survival as an important component of total energy expenditure. In the extreme, they lead to allostatic overload of one type or another. The most basic type of overload is a simple energetic shortfall, in which the body cannot acquire enough energy to meet its expenditure. A more complex type of overload accompanies sustained allostatic loads in individuals who can meet the energetic requirements. In these cases, the extension of altered hormonal and physiological states may lead to an increased chance of chronic or infectuous disease, psychological impacts, or other long-term health consequences. These consequences are the selective costs associated with the maintenance of elevated allostatic states; they are ultimately the reason why animals do not run at a higher energetic state all the time.

In the context of fossil hominids, I think this concept is important because it provides another piece of evidence that overall energy expenditure and other physiological variables cannot be predicted from body mass alone. Across much of human evolution, mortality risk across adulthood was significantly higher than in recent human populations. Humans lived in a broad range of environments, and at some times and places, they must have had relative resource abundance similar to, if not exceeding, that of the Upper Paleolithic and later Holocene people who had low adult mortality rates and elongated life histories. This is not to say that early humans would have matched the sustained population growth that commenced in the Late Pleistocene, but that at many times and places in the Early and Middle Pleistocene, such growth would have been probable for circumscribed times. Why did none of these people evidently live long and prosper to the extent seen later in the fossil record? A good answer (although not the only possible one) is that the real mortality risk came from the social factors. Absent direct violence (which did occur), the second most important social influence on health may have been allostatic loads of one kind or another.

This is not exactly news, since many paleoanthropologists have been investigating allostatic load for a long time (although usually under other names). For example, the energetic cost of pregnancy and lactation is perhaps the largest allostatic load faced by any humans as a nonpathological result of their biology. However, much in the study of social stresses in ancient humans has yielded to the wake of the observation that ethnographic hunter-gatherers are relatively egalitarian in social structure. This would appear on the surface to rule out the idea that there were major differences between people in their social status. But a relatively egalitarian structure only means that status differences were more fluid, not that they were less significant. A rigid pecking order can be distinguished easily on the basis of binary interactions between individuals. In contrast, fluid status distinctions depend on broader parts of the social network to resolve them. Such a system may result in a decreased total level of stress on lower-ranking individuals, but it need not do so. In early humans, there is no strong evidence that interpersonal relations fit the ethnographic hunter-gatherer model, but even if they did that is not sufficient to exclude the idea that significant allostatic loads occurred as a result of social interactions.

I might even offer a hypothesis that allostatic loads were driving factors behind the life history changes associated with the Late Pleistocene. At present, we know that major behavioral changes (at least in the circummediterranean region) included an increase in faunal dietary breadth, an increase in sedentism, growing population sizes and densities, and increased technological variability. All of these factors may reflect more basic changes in human interactions. In particular, they may correlate with a growing degree of social stratification and cultural differentiation. Together, these forces might have sharply increased the degree of competition for resources within social groups, while circumscribing to a greater extent the possibility of individual dispersal to other groups. In other words, the stress on lower ranking people could be expected to have increased while the opportunity to escape by moving would have decreased. If true, then allostatic load may have become an increasingly important factor at this time late in human evolution.

This hypothesis is potentially of great interest for the establishment of social systems predating the innovation of agricultural subsistence. A growing, less mobile, population would increase the opportunity for epidemic disease. The imposition of greater allostatic load might create a pool of individuals at greater risk for disease due to immune depression. Greater population pressure would have restricted both group fissioning and opportunities for dispersal. As a result, lower ranking individuals would be forced (to a greater extent than previously) to cooperate with people of higher status--possibly against their interest. Thus, people would have been forced away from egalitarian social structures into a more hierarchical organization. All of these forces are potentially synergistic, drawing an energetic load from lower-ranking individuals that would inhibit them from rising in the social hierarchy.

Were there energetic and disease factors contributing to the establishment of social hierarchies? It is clear that the very hierarchical nature of early civilizations must ultimately have arisen from simpler hierarchies in transitional societies of collectors, pastoralists, and early agriculturalists. Likewise, these societies represent a transformation of small-scale, egalitarian hunter-gatherer bands. But these transformations have usually been considered to result from purely social changes as a result of the network effects of accumulating wealth and increasing population size. Both of these factors were undoubtedly contributors.

Yet the idea that an accumulating health differential may also have emerged early in the prehistory of growing population size is appealing. Certainly people--especially men--would not tolerate the reproductive advantage of a few high-ranking individuals at their expense. By the origins of state-level societies, they simply had no choice: the accumulation of wealth and social influence of the highest-ranking kings, princes, priests, and other elite were strongly entrenched. But what enabled the initiation of hierarchicalization in earlier, smaller societies? People had no innate quest for wealth, since material wealth was entirely absent as we know it in all but the latest Pleistocene humans. Wealth was only a partial proxy for status, and was substituted for it only after accumulation of material goods became possible. But health was always a primary factor differentiating people. Mate choice in Pleistocene humans was likely highly influenced by health, with people strongly attuned to the health of potential partners. If status differences in growing populations led to a health differential, the innate ability to judge health in potential mates would tend to reinforce those status differences. In effect, the realized heritability of status (including this nongenetic effect) would increase; people would tend to inherit their status more and more from their parents. An initial chance hierarchy in status would snowball into one that was reinforced by biology.

Even so, small revolutions of the social order would have been common; just as large revolutions occurred later in human history. Ultimately people do not tolerate overarching power by a dominant elite, and they resist to the extent that social circumstances and material inequity will allow. This aspect of human nature must be the primary reason for the continuation of egalitarian social structure in hunter-gatherer groups. We can speculate that short-term hierarchies may have emerged in incipient form countless times during the Pleistocene evolution of humans. Resource shortfalls, group extinctions, and social fissioning would reverse this trend whenever it emerged. But the unique circumstances of the latest Pleistocene suspended many of the corrective mechanisms of small-scale hunter-gatherer bands. Human biology stepped into a new phase, from which only extreme technological changes would eventually begin to reclaim it.

References:

McEwen BS and Wingfield JC. 2003. The concept of allostasis in biology and biomedicine. Hormones and Behavior 43:2-15.

In the 2002 Annual Reviews in Anthropology, Leslie Aiello and Jonathan Wells provide a synopsis of the ways that morphological evolution in the human lineage have affected the energy utilization of our species and its ancestors. These considerations focus on body size, because it is tightly correlated with metabolic rates among mammals. Secondarily, they focus upon the relative sizes and proportions of different organs, especially the relative sizes of the brain and of the gut.

Aiello and Wells begin with the origin of early humans (which they assign to Homo ergaster). The most important change to happen at this time was an increase in body mass, likely to nearly twice the mass of female australopithecines. But there was also a complex of other changes that occurred at this time, including a change to more humanlike body proportions, with longer legs, and a change in diet toward higher energy food resources, probably including meat. One aspect of this change that the review summarizes is this our regulatory benefits of longer limbs, more linear physiques, and the effects of heat load upon a birthweight and energy expenditure during pregnancy, following the work of Wheeler (e.g. 1991), Ruff (1991), and Wells. From the increase in body mass, they calculate the necessary increase in resting metabolic rate following Kleiber's equations. They estimate that compared to Australopithecus afarensis, early humans would have required 39 percent more energy to meet resting metabolic requirements, with a much larger increase in females than males (resulting from the marked decrease in sexual dimorphism).

The authors spend a section considering what the dietary balance of these early humans must have been. They note that modern hunter gatherers with especially high energy requirements, such as Eskimos, meet these requirements by including a very high proportion of meat in their diets. Interestingly, they argue against this dietary model for the earliest humans, not on the basis of ecological reconstruction or arguments about scavenging vs foraging, but instead on the basis of the thermoregulatory requirements of meat digestion. They argue that digestion of meat produces more heat than the digestion of other kinds of foods, especially if the meat is protein-rich and fat-poor. They also note that the digestion of protein requires a great deal of water, which would be relatively scarce for savanna-based hominids. They do not use these arguments to suggest that early humans lacked meat in their diets, but instead emphasize that a balance between different dietary sources would be more advantageous, particularly if dietary fat were relatively unavailable.

Aiello and Wells then turn to the expensive tissue hypothesis. In brief, this hypothesis builds on the observation that some tissues require more energy for their resting metabolism than others. In particular nervous tissue is very expensive and digestive tissue is also quite expensive. The relative sizes of most body tissues are relatively constrained by functional requirements. But a reduction in dietary bulk might allow natural selection to pare away digestive tissues that were less necessary for food absorption, making energy available for the expansion of other tissues such as brain tissue (Aiello and Wheeler 1995). A novel element in this review is the inclusion of body fat and its potential complication in the estimation of resting metabolic rate. Aiello and Wells hypothesize that later members of the genus Homo were relatively fatter than earlier fossil hominids. It is well recognized that living humans in Westernized societies have a higher percentage of body fat than most mammals in wild populations. Fat tissue, called adipose tissue, has a relatively low contribution to overall metabolic rate. This means that an a fatter person will have a relatively lower metabolic rate than a leaner person of the same mass. If it is true that recent humans generally have been fatter than earlier humans, then even if their mass remained unchanged, the resting metabolic rates of human populations may have actually increased relative to their fat-free mass. This is a bit of a convoluted argument, dedicated to a single problem. Considering that recent humans have larger brains than their ancestors, the expensive tissue hypothesis predicts that either human metabolic rates must have increased over time, or that the relative mass of some other expensive tissues must have decreased. If humans became fatter at the same time that their brains increased in size, then the increase in fat mass might contribute to a relative reduction in the energetic requirements of the overall body mass. This reduction would have allowed an increase in the metabolic requirements of brain tissue. Aiello and Wells propose that these two opposing forces may have balanced each other, with the change in body composition underwriting the increase in size of the human brain.

Needless to say this vision is complicated by the fact that we have no evidence of soft tissue proportions in fossil humans. Likewise, there is no special reason to believe that recent humans--except for people in industrialized societies--actually are much fatter than their fossil ancestors. Aiello and Wells cite a study (Lawrence et al. 1987) that estimates body fat percentage in women in harsh environments at around 20 percent. This estimate would of course be higher for women than for men, considering the increased fat storage available in breast tissue and other sources in women. But it is far from clear that even human women have higher fat storage than females in other primate species. This is a subject that clearly needs further study.

There are several interrelated forces that do suggest that increased fat storage may have been an important human adaptation, possibly as early as the earliest fossil evidence of humans. One of these is the relatively high reproductive rate of humans compared to other hominoids. The short birth intervals of humans, combined with the rapid transition from weaning to new pregnancies among human mothers is significantly enhanced by the ability to store energy and smoothe out fluctuations in dietary resource availability. This hypothesis is supported by the observations that female reproductive fitness appears to depend on fat stores to some extent, and very thin women have a higher rate of miscarriage and a higher likelihood of low birthweight babies. Another is the fact that humans modify their group sizes with much less seasonal variation that is observed in chimpanzees.

Another novel element of this review is the consideration of energy costs as they change during early ontogeny. Aiello and Wells note that the metabolic costs of the brain are especially high very early in life, because of the early growth of the brain. They cite an estimate that the brain requires up to 70 percent of the total energy costs of the individual (Holliday 1986), although this sounds like an overestimate. They suggest that human children meet these energy requirements in part by compromising their rate of growth, especially during the time period between 2 and 12 years of age. The unique ontogeny of human growth in includes this time span during which chimpanzees actually have faster growth rates than humans, followed by the "adolescent growth spurt" in humans, when childhood growth rates continue and may even increase (Ulijaszek 1995). This alteration in rates may reflect the increased resting metabolic requirements of tissue proportions in human children. The authors also note that parent-offspring conflict provides another explanation for slowed growth rates in human children, considering that parents and children must both depend on the same resources, collected by parents. I might add to that the competition between children and new siblings, considering that at the weaning age it is likely that most human children would very shortly have seen their mothers investing their energetic resources in growing pregnancies and the care of subsequent offspring.

In the final section, the authors make suggestions about the relationship between energetic evolution and social organization. Citing Aiello and Key (2002), they provide estimates that indicate that lactating early humans would have had energy requirements 45 percent higher than lactating australopithecines, and "almost 100 percent higher than for a nonlactating and nongestating smaller-bodied hominin" (333). That paper argues that a reduction in the birth interval would have reduced the energy costs per offspring, at the same time that it increased overall reproductive output. The reduction is most noted in the length of lactation, which is the most expensive part of direct maternal investment. In that paper, they note that only a major shift in diet could allow this change to happen, because the resources lost to children by a reduction in lactation length would have to be replaced by other foods, presumably high-energy foods like meat. But they also note that other individuals besides the mother might be involved in providing these resources to children. They focus on the possible effects of grandmothers, following Kristin Hawkes and colleagues (1997). One might include on this list the possibility of paternal investment, or the contributions of other group members. In any event, the social changes necessary for effective hunter-gatherer foraging strategies, which necessitate the sharing of both risks and benefits of hunting, would help to support this strategy.

These energetic ideas leave several questions unanswered, mostly based around assumptions that cannot be verified. For example, what was the birth interval of australopithecines? If this birth interval were short, as in recent humans, then the transition to a more human-like body size might not been accompanied by such extensive social changes. And were the predecessors of early humans--such as Homo habilis--themselves fat? One might expect that the origins of tool use corresponded with the origins of some of the dietary changes that Aiello and Wells argued characterized early humans. If so, then energy storage must have been an integral element of this toolmaking adaptation. Indeed, the evidence the brain size first increase in Homo habilis or another small-bodied hominid directly detracts from the idea that energetic changes were the principal driving factors of changes in body size, sociality, or other early human characteristics. It goes without saying that we don't directly know what the proportion of different "expensive" tissues in australopithecines or any other early hominid might have been, beyond the suggestion that the reconstructed skeleton of Lucy had a broad gut and pelvic cavity.

References:

Aiello LC, Key C. 2002. The energetic consequences of being a Homo erectus female. Am J Hum Biol 14:551-565.

Aiello LC, Wells JCK. 2002. Energetics and the evolution of the genus Homo. Annu Rev Anthropol 31:323-338.

Aiello LC, Wheeler P. 1995. The expensive-tissue hypothesis: the brain and the digestive system in human and primate evolution. Curr Anthropol 36:199-221.

Hawkes K, O'Connell JF, Blurton-Jones NG, Alvarez H, Charnov EL. 1998. Grandmothering, menopause, and the evolution of human life histories. Proc Natl Acad Sci U S A 95:1336-1339.

Holliday MA. 1986. Body composition and energy needs during growth. In: Falkner F, Tanner JM, editors, Human growth: A comprehensive treatise, 2 edition. New York: Plenum. p 101-107.

Ruff CB. 1991. Climate and body shape in hominid evolution. J Hum Evol 21:81-105.

Ulijaszek SJ. 1995. Energetics and human evolution. In: Ulijaszek SJ, editor, Human energetics in biological anthropology. Cambridge, UK: Cambridge University Press. p 166-175.

Wheeler PE. 1991. The thermoregulatory advantages of hominid bipedalism in open equatorial environments: the contribution of increased heat loss and cutaneous evaporative cooling. J Hum Evol 21:107-115.