It's Curtains For The Expensive Tissue Hypothesis

From my previous post, you already know what a poor attempt at debunking the paleo diet looks like. Now, I figure I owe you an example of how to do it right. Call this a Thanksgiving present.

"Energetics and the evolution of human brain size," published earlier this month in Nature, tests and refutes the expensive tissue hypothesis. It's impressive work, and pretty devastating to the hypothesis that has provided a rhetorical foundation to the paleo diet mythology for over a decade now.

Navarrete's, et. al.'s, main findings (further details below) are:

• There is no negative correlation between brain size and gut size in any mammalian taxa, refuting the ETH's prediction to the contrary;
• There is, however, a strong negative correlation between brain size and adipose tissue deposits; that is, fatter animals have smaller brains than lean ones; and,
• Humans are seeming exceptions to this rule because our fat deposits don't interfere adversely with our means of locomotion, thus freeing up energy for encephalization that other primates have to use for carrying around all that fat.

And the stunning thing about this paper is that the authors didn't simply test the ETH using new data, but also re-tested the data from the original paper using newer statistical methods and controlling for confounding factors that that Aiello & Wheeler missed, for whatever reason.

Their conclusion: when adiposity, phylogenetic relationships, sample bias and sex differences are controlled for, Aiello's & Wheeler's original data don't support their hypothesis any better than the newer data does! In short, the ETH is wrong at the foundation, not just at the margins.

But, you should still hold your applause for a moment, so we can make clear not only what this paper is, but also what it is not.

It is not evidence that pre-humans were strict vegans. It is not evidence that Homo sapiens are natural herbivores. It is not evidence that meat and dairy, in themselves, are intrinsically either good or bad for us. If you're the kind of vegan who looks for an evolutionary hook to hang your fall-from-grace fantasies on, you'll have to look elsewhere. Prehistoric humans and their ancestors ate meat, and sometimes a heck of a lot of it. You'll just have to deal with that.

However, the paper is pretty good evidence that meat wasn't essential to our evolution. Meat, it turns out, probably didn't make us smart, after all. At the level of vegan blogosphere debate ammo, that might be cause for some applause.

The Original Problem
To understand how the ETH came about, how thoroughly Navarrete, et. al., have undermined it, and on what grounds they have done so, it's probably a good idea to hop in the Wayback Machine and understand what Aiello & Wheeler were trying to explain in the first place.

The $64,000 question in paleoanthropology (adjusted for inflation) for the last 80 years or so has been, "why can humans have such freakishly huge brains compared to other primates their size, but still have the same basal metabolic rate?" The question is rooted in a biological principle called Kleiber's Law, which demonstrates that the metabolic rate of most animals scales to the 3/4 power of their mass; this law holds true across the animal kingdom, and appears to function in plants and bacteria, too: even within individual cells themselves! Kleiber's law can be used to precisely calculate the metabolic rate of any animal just by knowing their total mass. In short, it shows that animals of roughly the same size will have roughly the same basal metabolic rate (BMR), and that's where the problem with humans comes in.

It turns out that within an animal, the metabolic rate is not evenly distributed among all its tissues. Some tissues -- brains, hearts, lungs, livers, the GI tract, to name a few -- use more calories than others; they are thus "expensive." Every organ has its own individual metabolic rate. So, even though animals of equal size will have equal overall BMRs, they won't necessarily allocate that energy to their organs in the same way.

Let's say you have two species of roughly equal mass. One of them is characterized by a super strong heart, and the other by advanced lung capacity. Hearts and lungs both use a lot of energy, so each species will allocate its overall BMR to its distinct tissues in different ways, but will still have the same total BMR as the other. This means that without a change in overall mass, the strong-hearted species can never have the amazing lungs of the strong breather, and vice versa. Kleiber's law must hold, and to do that, some organs and tissues have to take priority over others. So long as their overall BMRs remain the same, different species of equal mass can display a lot of variation in the ways their individual tissues consume energy.

This is the crux of the human brain problem.

Using Kleiber's law, Aiello & Wheeler noted that an 80-lb. australopithecine would have had roughly the same BMR as an 80-lb. Homo sapiens, despite the difference in their brain sizes. The human brain would have 4 to 5 times the metabolic cost of the softball-sized australopith brain. So, Aiello & Wheeler reasoned, in order to maintain the BMR predicted by our mass, humans must have made a trade-off between competing tissues at some point in our evolution; i.e., as our brains gobbled up more energy, some other set of tissues had to get less, and thus shrink over evolutionary time. Something had to give.

After assessing the cost and importance of various tissues within modern humans, Aiello & Wheeler concluded that the human tissue most reduced in comparison to other primates was the GI tract. As our brains got bigger, our guts got smaller. As a result, we had to become dependent on more high-quality, nutrient-dense, easily-digested food than other primates to maintain the high cost of our brains, since our reduced guts could no longer handle the sorts of food on which our ancestors had subsisted for millions of years. They proposed that the most likely reliable source of such calories was meat and other animal products. A dramatic increase in animal matter in the hominin diet eased the energy constraints imposed by nature on big brains, and allowed our brains to grow to massive proportions without violating Kleiber's law.

In the popular press and later, in the blogosphere, the short hand version of the ETH became, "meat made us smart," or "meat-eating made us human." But that's not precisely what Aiello & Wheeler were claiming, and the difference between what they claimed and what carnists who cite them claim is crucial to understanding what Navarrete, et. al., have accomplished with their new paper.

For the ETH, meat itself wasn't really the point. Though Aiello & Wheeler proposed it as the probable source of the necessary calories, they hinted that other high-quality foods, like sugary fruits, tubers, or oil-rich nuts and seeds, could also have done the job. A close reading shows that the ETH was fundamentally about total calories, not specific calorie sources. Even so, the prominence of meat-eating in the paper supplied de facto legitimacy to several paleofantasies about the necessity of meat to the human diet, one of which would become the modern paleo-diet movement.

But more fundamental to the ETH than meat-eating -- indeed, the whole point of the paper -- was the claim that Kleiber's law is maintained through a necessary trade-off between expensive tissues within a given organism, in this case Homo sapiens. Increased meat-eating was merely a consequence of this claim, not the foundation of it. And for the last 15 years or so, the argument over whether meat was important to our evolution has obscured the more fundamental -- and eminently more testable -- claim of an expensive tissue trade-off.

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.

The Fat Of The Matter
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.

To understand just how big of an impact bipedalism has on human energy expenditure, take a look at the paper's Supplemental Material, and its discussion of the different energy costs that excess fat imposes on humans and chimpanzees. Human foragers spend between 18 to 22 percent of their daily energy on locomotion. Chimps have a comparable but somewhat larger range of 16 to 30 percent. But, because of the different ways they move around, a 10 percent increase in body fat deposits for humans means only a 1 percent increase in needed energy, while for chimps it means a 2 to 3 percent increase.

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.

Digging Up Old Data
If Navarrete, et. al., had stopped there, they'd have a pretty strong case: the ETH's predicted negative correlation between brain size and organ mass appears not to exist, at least among mammals. But, they took their investigation a step further and decided to re-test Aiello's & Wheeler's original data set, controlled for several compounding factors that Aiello & Wheeler hadn't accounted for. And that's where the real knock-out punch to the ETH happens.

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).

In fairness to Aiello & Wheeler, most of this was beyond their control. 15 years ago, for instance, we didn't know that Paranthropus was a sister taxa to Homo rather than a direct ancestor, and the literature on primate body masses simply didn't contain as wide a sampling of platyrrhines as it does today. Aiello & Wheeler did the best they could with what they had.

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.

Taken together with the new author's own data, these re-testing results pretty much have put the ETH down for the count. If they want to save it, Aiello & Wheeler will have to tackle Navarrete, et. al., with much more rigorous data and analysis than they used the first time around. Make no mistake, this is a quiet revolution in action.

What this means to the vegan blogosphere is that there is now a robust and scientifically credible argument against the claim that meat-eating was essential to our evolution... and the case has nothing to do with animal rights or other aspects of vegan ethics. That being said, this paper cannot and should not be used as evidence that hominins did not eat meat at all, or that pre-human ancestors were purely frugivorous. If we do that with this paper, we'll be just as guilty of building a paleofantasy as the caveman dieters were when they turned the ETH into their shibboleth.

So, while you're dining on Tofurkey or some African pumpkin stew (my planned Thanksgiving meal) this holiday, and obnoxious Uncle Carnist breaks out the old meat-made-us-human canard for the millionth time, feel free to take him to the mat. He's had it coming for years.