Revisiting the Expensive Tissue Hypothesis

Or, I am bloody sick of talking about food reward.

A recently published paper in Nature is supposed to have demolished the expensive tissue hypothesis (ETH) proposed by Aiello and Wheeler. An excellent summary of why this paper supposedly demolishes ETH is given at the blog PaleoVeganology (yes, not all vegans are religious extremists). Since I don't have access to the full Nature paper, the PaleoVegan post will be my basic source of info on it.

Let's start with the original Aiello and Wheeler paper (or PDF). Here's the first paragraph of the abstract:

The brain is a very expensive organ in metabolic terms. Each unit of brain tissue requires over 22 times the amount of metabolic energy as an equivalent unit of muscle tissue. There is no correlation across mammals, however, between the relative size of the brain and the relative basal metabolic rate. The Expensive Tissue Hypothesis explains this apparent paradox by looking at the metabolic cost of the brain in the context of the costs of other metabolically expensive organs in the body. The results show that the increase in brain size in humans is balanced by an equivalent reduction in the size of the gastro-intestinal tract. In other words, the increased energetic demands of a relatively large brain are balanced by the reduced energy demands of a relatively small gastro-intestinal tract. This relationship also seems to be true in non-human primates.

And later on:

The gut is the only one of the expensive tissues that can vary in size sufficiently to offset the metabolic cost of the encephalized brain. This is because gut size is determined not only by overall body size but also by diet. Gut size is associated with both the bulk and digestibility of food. Food of low digestibility requires relatively large guts with elaborated fermenting chambers (stomach and/or small intestine) while food of high digestibility (such as sugary fruits, protein and oil rich seeds and animal material) requires relatively smaller guts characterised by simple stomachs and proportionately long small intestines.

So the crux of their hypothesis is a negative correlation between brain size and gut size.

Now let us examine the Navarrete et al paper. Here's the abstract:

The human brain stands out among mammals by being unusually large. The expensive-tissue hypothesis¹ explains its evolution by proposing a trade-off between the size of the brain and that of the digestive tract, which is smaller than expected for a primate of our body size. Although this hypothesis is widely accepted, empirical support so far has been equivocal. Here we test it in a sample of 100 mammalian species, including 23 primates, by analysing brain size and organ mass data. We found that, controlling for fat-free body mass, brain size is not negatively correlated with the mass of the digestive tract or any other expensive organ, thus refuting the expensive-tissue hypothesis. Nonetheless, consistent with the existence of energy trade-offs with brain size, we find that the size of brains and adipose depots are negatively correlated in mammals, indicating that encephalization and fat storage are compensatory strategies to buffer against starvation. However, these two strategies can be combined if fat storage does not unduly hamper locomotor efficiency. We propose that human encephalization was made possible by a combination of stabilization of energy inputs and a redirection of energy from locomotion, growth and reproduction.

The heart of the matter seems to be related to fat storage and human's bipedal locomotion. To quote from PaleoVegan:

In other words, it costs chimps twice to three times as much energy to move around the same amount of body fat as a human. Further complicating the matter is that the energy cost of travel during climbing for primates is almost directly proportional to body mass. Quadrapedal terrestrial walking and briachiation as modes of transport simply impose higher costs on primates than does efficient bipedalism. This energy cost adds up over time (especially evolutionary time), and thus can constrain the total amount of BMR available for encephalization. Thus, because humans save so much energy by being bipedal, they can store relatively large amounts of adipose tissue and still grow big brains.

So a fat human can walk around much more efficiently than a fat chimp, that means that just by walking on two legs humans could put that extra energy into our big brains. For me this raises the obvious question: don't chimps spend most of their time locomoting with their arms? Again, I don't have full access to the paper but it seems like apples and oranges. The biggest advantage to a bipedal hunter-gatherer existence as far as nutrient dense foods is the hunting, not the gathering, nor the increased efficiency of being able to carry around more fat.

What the Navarrete et al paper did was to remove adipose tissue from the equation to take into account the efficiency variation of adipose tissue and the efficiency of terrestrial movement. Another thing they decided to do was to test the ETH hypothesis across a variety of animals instead of just primates.

Again from PaleoVegan:

Any good hypothesis can produce at least one testable prediction. And the ETH has one, right there for everyone to see (though it's been astonishingly ignored for 15 years). If the ETH is true, we should expect to find a tight negative correlation between brain mass and the mass of other expensive tissues across a range of taxa, not just among primates. And it's this prediction, not whether cavemen were meat-eaters, that Navarrete, et. al., set out to test.

I would qualify that first sentence as any real scientific hypothesis has to be able to produce a testable prediction. Otherwise we are just talking about mysticism. But the devil is in the details. I can form what I think is a testable prediction of a hypothesis that is mistaken based on my assumption.

PaleoVegan:

The key way they tested the overall hypothesis across various mammal groups was controlling for adipose tissue deposits in their calculation of a given animal's mass. In short, they omitted fat deposit mass from all specimens, eliminating it as a variable. This was an important control tactic (and one not used by Aiello & Wheeler in their original paper), because adipose mass varies by season and habitat among many species, and can thus be a major confounding variable. Only by eliminating it altogether and testing brain size against fat-free body mass, the authors reason, could a possible trade-off between tissues be reliably detected.

Under these conditions, no negative correlation between brain size and digestive tract mass was found. In fact, no negative correlation was found between brain size and the mass of any expensive tissue. The authors did, however, uncover a tight negative correlation between brain size and adipose tissue depots: the fattest species had the smallest brains.

Given Kleiber's law, this might at first look like a dilemma: fat tissue doesn't use a whole lot of energy, so why would it constrain brain size? The answer is that it costs an animal a lot of energy to lug the extra weight around, especially while climbing or running. And it's here that humans -- along with whales and seals -- have an advantage: fat stores don't significantly interfere with our ways of getting around. Bipedalism and dorso-ventral flexion (the swimming method used by cetaceans and pinnipeds) are simply more efficient ways of moving.

So humans are more efficient runners? No, humans are more efficient at running with fat. Navarrete et al believe that this is an important advantage that needs to be controlled for.

This paper, The Energetic Paradox of Human Running and Hominid Evolution has this to say about the efficiency of human running:

The energetic cost of transport (oxygen consumption per unit body mass per unit distance traveled) for running humans is relatively high in comparison with that for other mammals and running birds. Early comparative studies showed that a mammal the size of man should consume roughly 0.10 ml of oxygen per gram body mass per kilometer traveled, but the measured value for man is over twice this amount (0,212 ml) A recent analysis of 64 species of running birds and mammals confirms the initial observations that the cost of transport is relatively high for human runners.

First of all I'd like to bring up what seems to me like a glaring hole in the Navarrete et al bipedal lipid tissue efficiency argument: terrestrial birds are bipedal, and they aren't exactly famous for having large brains. What's another huge difference between ostriches and human hunter-gatherers? Diet. An ostrich consumes, according to Wikipedia, "... seeds, shrubs, grass, fruit and flowers; occasionally they also eat insects such as locusts." In other words, everything you'd expect to see at your local vegan restaurant, minus the locusts, of course. None of it famous for being nutrient dense, with the possible exception of fruit.

Navarette et al go on to re-test Aiello and Wheelers original paper with updated data, which PaleoVegan considers to be the knock-out punch for ETH. PaleoVegan writes:

As detailed in the Supplemental Material, Aiello & Wheeler were working with a data set that had a couple of problems. Namely, it was biased towards catarrhine primates over platyrrhines; it didn't control for sex differences between members of species with marked sexual dimorphism (sexual size dimorphism affects body mass more than brain size), or for differences in the body mass of wild vs. captive specimens of the same species; and it didn't account for phylogenetic relationships between various hominid species (a fact I have pointed out before).

[...]

Nevertheless, Navarrete, et. al., were able to identify and control for these confounders in a new test using the latest phylogenetic statistical methods on the original data sample. And the results did not support Aiello's & Wheeler's hypothesis; even their own data failed the ETH in the end.

Now I don't have access to the data or even the full paper so I can't really judge this, and I frankly wouldn't be qualified to judge it even if I did.  I would simply add that if this specific expensive tissue hypothesis has been disproven (ratio of expensive tissue gut length to expensive tissue brain size) that doesn't mean that all expensive tissue hypotheses are hereby rendered invalid, or that parameters can't be changed for this one. As I pointed out in the comments over at PaleoVegan:

The Humane Hominid [in response to Anand Srivastava]:

"Also, you don't get to change the ETH's parameters in order to save it"

I'm no expert in biological science, but in physics hypotheses and theories have their parameters modified or even added and subtracted all the time. When Einstein added in the parameter of the cosmological constant in 1917 to General Relativity, GR could have been more considered a hypothesis not a theory, as its predictions had not been experimentally tested (perihelion precession of Mercury had been observed long before GR). http://en.wikipedia.org/wiki/Cosmological_constant

But beyond this quibble I think PaleoVegan did an admirable and even-handed job of summarizing the Navarette et al paper. Do I think this destroys ETH? No. I'm pretty convinced that nutrient dense food, especially animal fat, was the key to human encephalization.