Lesser mammals, with higher levels of energy expenditure relative to body size than primates.

One of the recurring motifs in any intro-level Human Evolution class is the importance of bipedalism.  I’ve tried to teach this topic in a variety of ways, even going so far as to encourage undergrads to walk like chimpanzees – torso swaying laterally, knees slightly bowed, spine kyphotic. For some reason, they never seem to want to do this in front of their peers. However, one of the easiest ways to get students to appreciate our unique form of locomotion is to emphasize the amount of energy we save by striding around on two legs. Bioenergetic studies since the 1980s have demonstrated that when it comes to locomotor efficiency, we’re actually doing pretty well for ourselves as a species. Humans  are at least on par with other quadruped mammals when it comes to locomotor efficiency, and human bipedalism is even more energetically efficient than chimpanzee locomotion  (Rodman and McHenry, 1980).

Net Cost of Transport Relative to Body Mass in Chimps and Humans (from Sockal et al., 2007). Dashed lines demonstrate trends from birds and other mammals.

However, recent research is indicating that we’re not only efficient when it comes to our locomotion – we also appear to have far lower rates of overall energy expenditure than other mammals (Pontzer et al., 2014). Herman Pontzer, a professor at Hunter College, recently came and gave a talk at Michigan as part of the Evolution and Human Adaptation lecture series. His lecture showcased some of the major findings that have come out of recent research into primate energetics. After jokingly noting that a bioenergetic approach holds the view that “life is just a game of turning energy into kids” he embarked on a discussion of the surprising evidence for primate uniqueness when it comes to energy expenditure. He structured his talk relative to two main points:

1. Primates seem to have relatively low levels of daily energy expenditure, even when the effects of activity, phylogeny and body size are controlled for.

Based on Kleiber’s law, an animal’s Basal Metabolic Rate (BMR) should be 3/4 the power of an animal’s mass, which shows up as a straight line on a log-log plot (Kleiber 1947). BMR is the amount of energy expended when an organism is at rest – it’s enough to keep you alive and awake, but nothing more. Importantly, though BMR is often used as an index of Total Energy Expenditure ( a measurement of an organism’s total energy budget or kcal/day), BMR in fact only accounts for half of TEE  in most mammals. Additionally, BMR is unrelated to important life history traits like aging, growth rates or reproduction in mammals when other factors like body mass and relatedness are held constant (Pontzer et al., 2014). Because primates have notoriously unique life history patterns, with slower rates of reproduction, growth and aging than other mammals, Pontzer and his colleagues decided to examine how primates ranked when it came to energy expenditure.

To do this, they measured CO2 output in primate subjects using  isotopes of hydrogen and oxygen in doubly labeled water, a process that allowed them to calculate the metabolic rate of various primate species. Their test subjects ranged from ring-tailed lemurs to orangutans to humans, covering the full range of body sizes and taxonomic scope of the order in order to control for phylogeny and body size. They also measured energy expenditure in both captive and wild primates, as well as in sedentary western populations and more active foraging populations. Their results showed that primates shared the same relationship between TEE and body mass as other animals, but that the line of fit was significantly lower. This suggests that TEE is lower in primates than it is in other mammals, even after body mass is controlled for.

Log-Log Graph of Primate TEE vs. Body Mass, relative to non-primate mammals. This is from the Pontzer et al 2014 PNAS article, figure itself stolen from Scilogs)

In fact, primates only need 50% of the calories that you would expect based on the energy requirements of other mammals of equivalent size. For example, most humans need around 2,500 calories to go about their daily business.  Springboks, a type of African antelope with a comparable body mass to humans, need 5,800 calories to power through each day. What this means is that for a human to get their levels of energy expenditure up to that of a typical non-primate mammal, they’d have to run a marathon.

As a visual aid, I have helpfully converted the nutritional requirements of springboks and humans into the equivalent quantities of large cheese pizzas.

What’s also noteworthy about humans is that these low levels of DEE don’t change significantly as a result of differences in  lifestyle or activity patterns. The Hadza are a group of  hunter-gatherers living in northern Tanzania, whose subsistence strategy involves a far more active lifestyle than the sedentary 9-5 desk jockeying that characterizes many North American populations. Like the !Kung San of South Africa, the Hadza have been persistently plagued by swarms of anthropologists for the last century, which made the establishment of the Hadza Energetics Project possible. When Pontzer and his colleagues compared the Hadza DEE levels to those of more sedentary European and American populations (controlling for lean body mass), Hadza levels of daily energy expenditure were strikingly similar to those of the other groups.  Pontzer underscored that the energy costs of activities like walking, as measured in kcal/km, were also similar across populations, so the Hadza weren’t “doing more with less”. Instead they were likely allocating their energy differently. Strikingly, while over 3/4 of the Hadza are smokers, and their diet is high in both meat and sugar, levels of cardiovascular disease are low. Accordingly, Pontzer hypothesized that this group might be spending more of their overall DEE on physical activity, rather than vascular infrastructure or the disease burdens that characterize other populations.

Anthropologists: Asking you invasive questions about what you’re eating since the 18th Century                           (Richard Lee with the !Kung San, likely during the 1960s-70s)

Strikingly there’s also  some new evidence that haplotype groups have a significant impact on DEE levels (when the effect of body mass is controlled for). These findings suggest that daily energy expenditure in humans isn’t determined by activity levels, but is instead shaped by population specific physiological constraints. That’s not to say that we should all immediately cancel our gym memberships, since exercise has a range of other proven physiological benefits. As Pontzer quipped  “[Excercise] is not going to make you skinny, but it might still make you not dead”. This pattern isn’t only true for our species, but seems to characterize the order primates generally. Indeed, the authors of the 2014 PNAS piece note that “[r]ather than low levels of physical activity, the magnitude of difference in primate TEE suggests a systemic reduction in cellular metabolism” (Pontzer et al., 2014: 1434).

2. Primate life history patterns  are likely related to our lower levels of energy expenditure.

One hypothesis to explain senescence, or aging, is that it results from accumulated cellular damage over time. Since TEE is also reflective of cellular metabolic rates (with higher TEE correlated with an increased number of kcal per cell per day), then lower TEE and lower cellular metabolic rates might stave off the accumulation of such damage for longer timespans. As Pontzer et al., note, if the number of cells per gram of body mass (M) is constant across species, then (TEE/M) is proportional to mortality rates, and (M/TEE) is proportional to maximum lifespan. In short, this explanation for senescence predicts that organisms with lower levels of TEE will show decreased mortality rates and increased maximum lifespans relative to organisms with higher levels of TEE. These predictions are borne out by the team’s study of TEE in primates relative to non-primate mammals, especially when their long lifespans are taken into account. The same pattern holds true for reproduction and growth. Normally, body mass is used as a means of predicting an organism’s rate of production, causing primates to show up as outliers with slower rates of growth and reproduction than other mammals. However, when TEE is used instead to predict rates of production, “…primate reproductive output and growth rate are similar to those of other eutherian mammals when plotted against estimated TEE” (Pontzer et al., 2014: 1435).

All of this evidence led researchers to conclude that the slow growth and long lives of primates may be related to our low energy throughput, which itself shapes our life history. This has important implications for public health policies today. Because it appears that evolution has selected for the low levels of DEE in primates, it’s possible that the only way to lose weight efficiently is to watch your calorie input, since energy throughput will remain broadly similar,  no matter your activity level. As Pontzer noted during the question and answer session, “over the course of evolution, losing weight has always been a bad thing, whether you’re a trilobyte or a fruit fly or a chimp. You could argue that the past six hundred million years of evolution have in fact been devoted to figure out ways NOT to lose weight”.

Exactly, red ruffed lemur, exactly. Your DEE is too low for cupcakes.

All in all this was a fascinating talk. I’m particularly curious about the issues of energy allocation Pontzer touched upon. If higher activity levels don’t increase DEE in humans, that means periods of higher activity levels must be “paid for” by the same energy budget allotted to periods of lower activity levels. The deficit has to come from somewhere, and one of the most interesting ways to focus on this may be to carefully examine pathways of energy allocation in professional athletes. I’m excited to see what direction bioenergetics researchers head in next.

On a personal level,however, I plan on using this newfound knowledge of human bioenergetics to craft some sort of cogent explanation as to why I allocated a large portion of my energy budget to writing this blog post instead of working on my dissertation.

References

Rodman PS, & McHenry HM (1980). Bioenergetics and the origin of hominid bipedalism. American journal of physical anthropology, 52 (1), 103-6 PMID: 6768300

Kleiber, M. (1947). Body Size and Metabolic Rate Physiological reviews, 27 (4), 511-541

Pontzer H, Raichlen DA, Gordon AD, Schroepfer-Walker KK, Hare B, O’Neill MC, Muldoon KM, Dunsworth HM, Wood BM, Isler K, Burkart J, Irwin M, Shumaker RW, Lonsdorf EV, & Ross SR (2014). Primate energy expenditure and life history. Proceedings of the National Academy of Sciences of the United States of America, 111 (4), 1433-7 PMID: 24474770

Image Credits: Sleeping dog and cat found here. Figure 1 is taken from Sockol, Raichlen and Pontzer’s 2007 paper in PNAS. Graph of TEE vs. body mass is proximately from scilogs.com, but ultimately from the Pontzer et al. 2014 paper in PNAS. Image of springbok found here. Image of cheese pizza found here. Photo of Liz Lemon from sidereel. Richard Lee photo taken from Encylopaedia Britannica Kids, or all places. Appalled lemur is from Sugarland Cupakes (taken at the Duke Lemur Center).