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William Collins
An imprint of HarperCollinsPublishers 1 London Bridge Street London SE1 9GF WilliamCollinsBooks.com This eBook first published in Great Britain by William Collins in 2020 First published in the United States by Houghton Mifflin Harcourt in 2020 Copyright © David Raubenheimer and Stephen J. Simpson 2020 Cover images © Shutterstock David Raubenheimer and Stephen J. Simpson assert the moral right to be identified as the authors of this work. A catalogue record for this book is available from the British Library. All rights reserved under International and Pan-American Copyright Conventions. By payment of the required fees, you have been granted the non-exclusive, non-transferable right to access and read the text of this e-book on-screen. No part of this text may be reproduced, transmitted, down-loaded, decompiled, reverse engineered, or stored in or introduced into any information storage and retrieval system, in any form or by any means, whether electronic or mechanical, now known or hereinafter invented, without the express written permission of HarperCollins. Source ISBN: 9780008359218 Ebook Edition © June 2019 ISBN: 9780008359232 Version: 2020-02-26
To Jacqueline, Gabriel, Julian, Jan, and Fred
–DR
To Lesley, Alastair, Nick, and Jen
–SJS
Contents
Cover
Title Page
Copyright
Dedication
Introduction
1. The Day of the Locusts
2. Calories and Nutrients
3. Picturing Nutrition
4. Dance of the Appetites
5. Seeking Exceptions to the Rule
6. The Protein Leverage Hypothesis
7. Why Not Just Eat More Protein?
8. Mapping Nutrition
9. Food Environments
10. Changing Food Environments
11. Modern Environments
12. A Unique Appetite
13. Moving the Protein Target and a Vicious Cycle to Obesity
14. Putting Lessons into Practice
More on Nutrients
Acknowledgments
Further Reading
Index
About the Author
About the Publisher
Introduction
Stella lived in a community on the outskirts of Cape Town, South Africa. She was one of twenty-five adults who between them had an impressive forty children. It was a serene setting on the foothills of Table Mountain, surrounded by vineyards, pine plantations, groves of eucalyptus trees, stretches of natural fynbos vegetation, and a few suburban settlements.
Caley Johnson was a young anthropology student from New York City. Her graduate thesis was on nutrition of a rural population in Uganda, who lived almost entirely off natural foods. Her advisors suggested that it would be an interesting comparison to include in the study a population that ate not only natural foods but also some sugary and fatty processed foods. This is what brought Caley to Cape Town, where she and Stella met.
Caley’s research approach, standard for her field, involves watching individuals throughout an entire day and recording which foods they eat and how much of each. The foods are then analyzed in a laboratory for their nutrient content to give a detailed daily record of the diet. But this study was radical in one respect: rather than follow several subjects, each on a separate day, the team had decided to study the diet of only one individual for thirty consecutive days. Caley therefore came to know Stella and her eating habits intimately.
What she saw was intriguing. Stella’s diet was surprisingly diverse: she ate many foods, almost ninety different things over thirty days, and on each day, she ate different combinations of natural and processed foods. This suggested that Stella was not particularly discerning, indiscriminately eating whatever she fancied. The numbers from the nutrient laboratory appeared to tell the same story. The ratio of fats to carbohydrates in Stella’s diet varied widely, as might be expected given the variety of foods that she ate and how these differed from one day to the next.
Then Caley noticed something unexpected. When she totaled the combined calories from carbs and fats each day and plotted that figure on a graph against the amount of protein consumed each day, there was a tight relationship. This meant that the ratio of protein to fats and carbs—a very important measure of dietary balance—had remained absolutely consistent over the course of an entire month, regardless of what Stella had eaten. What’s more, the ratio that Stella had eaten each day—one part protein to five parts fats and carbs combined—was the same combination that had been proven to be nutritionally balanced for a healthy female of Stella’s size. Far from being indiscriminate, Stella was a meticulously precise eater who knew which dietary regimen was best for her and how to attain it.
But how did Stella track her diet so precisely? Caley knew the complexities of combining many foods into a balanced diet—even professional dietitians have to use computer programs to manage this. Could it be, she might have been forgiven for wondering, that Stella was secretly an expert in nutrition? Except that Stella was a baboon.
A confounding story, when you consider all the dietary advice we humans seem to require in order to eat properly (not that it does most of us a lot of good).
Meanwhile, our wild cousin, the baboon, apparently has figured it all out by instinct. How could such a thing be so?
Before we begin to explore that question, here’s another tale, even weirder. It starts with a lab scientist named Audrey Dussutour at the University of Sydney. One day Audrey took her scalpel and started preparing an experiment by cutting a gooey blob of slime mold into small pieces. Beside her on the bench sat hundreds of Petri dishes, all set out neatly in rows.
Audrey picked up each fragment of yellow goo with forceps and carefully transferred it into the center of a dish, then covered it with a lid. The dishes contained either small blocks of protein or carbohydrate, or a wheel of eleven tiny bits of jelly-like food medium varying in the ratio of protein to carbs. Once all dishes had received their bit of slime mold, Audrey stacked them in a large cardboard box and left them overnight.
The next day, she opened the box and laid out the dishes again on the bench. When she looked closely, she was astonished. Each bit of goo had changed overnight. When the slime molds were offered two blocks of food—one of protein, the other of carbs—the blobs extended their growing tendrils to both nutrients, reaching out just far enough in each direction to pull in a mix of the two. That mixture contained precisely two parts protein to one part carbs. Even more incredibly, when bits of goo were placed in dishes containing eleven different food blocks, the tendrils grew overnight from the center of the dish to colonize only the blocks containing that same two-to-one nutrient mixture, ignoring the rest.
What is so special about a diet of two parts protein to one part carbs? The answer came when Audrey placed pieces of slime mold into dishes containing differing combinations of protein and carbohydrate. The next day, some bits of slime remained stunted, whereas others had grown dramatically, extending themselves across the dish in a lacy network of pulsing yellow filaments. When Audrey later mapped the growth of the blobs, it was as if she had charted the up-and-down contours of a mountain. Goo placed on a nutrient that was two parts protein to one part carbs sat at the summit of the growth mountain. As the proportion of protein fell and carbs rose, or vice versa, the blobs’ growth decreased. In other words, when the bits of slime mold were given the chance to select their own diet, they chose precisely the mixture of nutrients needed to optimize healthy development.
Audrey’s yellow goo with the remarkable nutritional wisdom is a creature with the scientific name Physarum polycephalum—literally, many-headed slime. It is the real-life version of The Blob of B-movie fame. It is seldom seen, but like other slime molds (including the wonderfully named dog’s-vomit slime mold) and fungi, it lives a secretive life among the leaf litter, logs, and soils of the world’s forest floors. It is a single-celled creature with millions of nuclei, which can regenerate itself from tiny pieces, crawl like a giant amoeba, and grow its own complex, reticulated architecture of tubes that pulse and distribute nutrients around its network. It simply creates tentacles and then reaches out with them to grab whatever it wants to eat. Fascinating, if a little horrifying.
Now, we may be able to accept that Stella the baboon can make some wise nutritional decisions. But how can a single-celled creature without organs or limbs, let alone a brain or a centralized nervous system, make such sophisticated dietary choices and then carry them out?
This puzzled us, too, so, we asked an expert.
Professor John Tyler-Bonner passed Steve a laboratory beaker filled with steaming coffee, freshly brewed on the naked blue Bunsen burner flame that hissed quietly on the teak benchtop. Steve sat discussing Audrey’s results with this venerable guru of slime mold biology in John’s office—a time capsule that has not been refurbished since 1947, when John first arrived on faculty at the Department of Ecology and Evolutionary Biology at Princeton University. He pioneered the study of slime molds, and his work has helped lay the foundation for the study of complex decision-making within distributed entities, such as bird flocks and fish schools, crowds of people, or global corporations.
John explained that each part of the blob senses its local nutritional environment and responds accordingly. As a result, the entire blob acts as if it is a single sentient being, seeking out optimal sources of food—a balanced diet that will ensure favorable health—and rejecting what does not serve that goal.
This, you may agree, is better than what is achieved by some other sentient beings we could name. And this, as you probably realize by now, has everything to do with the subject at hand.
Why have we, two entomologists, written a book about human diet, nutrition, and health, a subject on which quite a few experts have already weighed in (no pun intended)? We didn’t start out meaning to do any such thing. Throughout our lives as scientists, and especially during the first two decades of our thirty-two-year collaboration, we have studied insects in an attempt to solve one of nature’s most enduring riddles: How do living things know what to eat?
Answer that and you’ve learned something very important—possibly even useful—about life itself. And not just for insects. But we’re getting ahead of ourselves now. Better to start at the beginning.
1
The Day of the Locusts
THE YEAR IS 1991. WE ARE SITTING TOGETHER AT Steve’s computer in his office in the Oxford University Museum of Natural History—the same place that in 1860 hosted the “great debate” over Darwinian evolution between Thomas Henry Huxley and the Bishop of Oxford, Samuel Wilberforce. That legendary encounter is best remembered for a heated exchange in which Wilberforce supposedly asked Huxley, who was known as Darwin’s “bulldog,” which of his grandparents was descended from monkeys. Huxley is said to have replied that he would not mind having a monkey as his ancestor, but he would be ashamed to be related to someone who used his great gifts to obscure the truth.
We had just performed the biggest dietary experiments we’d ever attempted. The study involved locusts, which are a special type of grasshopper and, as we will explain below, the ideal animal for our study.
Little did we know that before our session that day was over, the seeds for a new approach to nutrition, one heavily dependent on Darwin’s theory, would be sown.
We wanted to answer two questions. First, do animals decide what to eat based on what’s best for them? And second, what happens if for some reason they fail to follow that diet and eat another one instead?
You can see how these answers might be somewhat important.
Twenty-five foods had been carefully prepared in the lab to differ in the balance of protein to carbs, the two main nutrients consumed by herbivorous insects such as locusts. The foods ranged from high protein/low carb (a bit like meat) to high carb/low protein (more like rice) and everything in between.
Despite their varying compositions, the foods all looked very similar: they were dry and granular, a bit like cake mix before adding the liquid. The insects seemed to like them.
The mixtures were fed to the locusts, each of which could eat as much as it liked, but only of the single food it was given, until it molted to become an adult. This took a minimum of nine days and up to three weeks, depending on the food. Logistically, then, quite a challenge—painstakingly preparing twenty-five different foods, feeding one to each of two hundred insects, and then meticulously measuring how much every individual had consumed each day.
During the experiment, we spent what felt like endless hours together deep in the bowels of the Zoology Department in a cramped, humid room heated to 90 degrees Fahrenheit—a temperature at which desert-living locusts thrive but which can test a human friendship. Music helped—John Cale and Talking Heads kept us sane. Each locust lived within its own plastic box, with a metal perch to rest upon, a small dish of its assigned food that had been weighed to the nearest tenth of a milligram, and a water dish.
Every day we had to remove each locust’s food dish and, like meticulous sewerage workers, pick out any pellets of locust poo from the food dish and box. We measured how much was eaten and digested by weighing food dishes before and after feeding and analyzing excrement. Every food dish had to be placed in a desiccator to dry off any moisture and was then reweighed on a set of electronic scales that could detect a change of one hundred thousandths of a gram. By measuring the difference in weight of the food dish before and after feeding, we calculated how much the insect had eaten that day, and from that we could determine exactly how much protein and carbs it had consumed.
We did this for all two hundred locusts day after day until they either successfully molted to become winged adults or died beforehand. We recorded how many days that took, measured the animal’s weight, and analyzed how much fat and lean tissue they had grown.
And then, at last, we were side by side at Steve’s computer, about to learn the results of the experiment. In order to understand the results, we should first take a look at locusts in their natural context. After all, they didn’t evolve while living in a basement lab at Oxford. And, as we show throughout this book, nothing about nutrition makes sense unless you understand the biological context in which the species evolved, ours included.
Two juvenile locusts, somewhere in North Africa.
One grew up on her own. It hasn’t rained locally for months, and other locusts are few and far between. She is a beautiful shade of green, which allows her to blend in with the vegetation. She has a solitary existence, being shy in her behavior and repelled by other locusts. For good reason: one locust can hide; larger groups will attract unwanted attention from hungry birds, lizards, and hunting spiders.
Elsewhere, another locust was reared in a crowd. It rained not so long ago, and others like her are around in large numbers, feasting on the abundant vegetation. She is a party animal—brightly colored, very active, and attracted into groups. These aggregations form marching bands, and when they become winged adults, flying swarms that migrate across vast areas of Africa and Asia. A plague of the desert locust in North Africa can contain hundreds of billions of insects and eat as much in a single day as the entire population of New York will in a week. When they move into agricultural areas, they are devastating (locusts, not New Yorkers).
The two locusts are not different species (as was thought originally)—they could even be sisters. Every one of their kind has the potential to become either a shy green grasshopper or a gregarious extrovert, depending on whether they grow up alone or in a crowd. The process of changing from one form to the other occurs quickly. If you took the solitary green grasshopper and put her in a crowd, within an hour she would be attracted rather than repelled by other locusts, and a few hours later she could be part of a marching band. Before long she will change from green to being brightly colored.
This transition is known as density dependent behavioral phase change, and Steve’s research group spent years trying to understand it.
One of the initial questions we had was this: What is it about being in a crowd that causes the change? What stimuli are provided by other locusts that might trigger the transition? Could it be the sight of them, their smell, their sound?
As we discovered, touch is what’s critical. When there is a limited availability of suitable food plants, solitary locusts are forced to forage nearer each other than they’d prefer. The congregated insects jostle one another, and this physical contact causes the change from repulsion to attraction.
Once enough gregarious locusts come together, suddenly, as if of one mind, the entire group becomes highly aligned and starts to march.
We found that the collective decision to start marching emerges within a crowd from simple local interactions among locusts. In other words, there is no leader locust or hierarchical control. Marching emerges because the locusts are all following one easy rule: “align with your moving neighbors.” Once a critical density of locusts is reached, just adding one or two more will suddenly cause the transition to collective, aligned movement. The terrible march has begun.
Of course, we still didn’t understand why locusts should follow the simple rule to align with their moving neighbors. We suspected that nutrition may play a role—as it does in most things. The answer came from our study of a related animal called the Mormon cricket, and it turned out that their motive was rather sinister.
The Mormon cricket is a large, flightless insect built like a small tank that lives in the southwestern United States and forms vast marching swarms extending miles. They are called this because they began to devastate the first crops planted by the Mormon pioneers after arriving at Salt Lake in 1848. The community was powerless to stop the destruction and were facing starvation until, in the nick of time, a flock of seagulls came to the rescue and ate the crickets. There is now a monument to the gulls commemorating this event at the Temple in Salt Lake City. The seagull is the state bird of Utah (an odd thing, considering that it’s landlocked, but gulls find their way to any large body of water).
Steve was in Utah, studying swarms of Mormon crickets with colleagues Greg Sword, Pat Lorch, and Iain Couzin, when they discovered the reason behind its sudden decision to align and begin marching. As Steve explains:
We were staying in a truck stop motel, eating junk food washed down with Polygamy Porter (slogan: “Why have just one?”). The crickets were about in huge numbers. Greg and Pat had radio-tracked vast bands moving up to two kilometers each day through the spectacular sagebrush country.
Here’s a clue to why all those crickets were migrating. We recorded a single band of them crossing a main road for five continuous days. When they got squashed by cars, those following behind stopped to eat the corpses. And got squashed by cars. Before long, the mess was ankle deep, and snowplows had to be dispatched to clear the greasy slurry.
But why might herbivorous insects so avidly eat one another, even to the point of mass suicide? After all, with lots of vegetation around, there were plenty of other things for them to consume.
We had brought along to the desert the same dry, powdery feeds used in our big locust study back at Oxford, and we laid dishes of it out in front of the marching cricket bands.
The result was revealing. The crickets ignored the dishes of high-carb food but stopped to eat from the ones containing protein.
And aside from our little buffet, what was the nearest source of high-quality protein to those crickets? The cricket in front. What was forcing the march was simple: if you don’t move forward when your neighbors to the rear do, they will eat you. Meanwhile, of course, if the creature in front of you stops, you may seize upon it as a meal. Cricket cannibalism was driven by a powerful appetite—for protein.
And we discovered that locust habits can be equally gruesome when it comes to hungering for that nutrient. We learned this inadvertently, when Steve was trying to explore the signals that tell locusts when they are full during a meal. In an experiment, he had laboriously cut the nerves carrying feeling from the end of the insects’ abdomens to their brains. After the surgery, he put all the locusts in the same box to recover. Next morning, when Steve looked, he saw that none of the locusts had a body left below the point where the nerve had been cut. The insects had formed a kind of daisy chain, chewing off the hind end of the locust in front (who couldn’t feel a thing) while at the same time having its own numbed abdomen eaten by the locust behind.
What better animal, then, to use for testing big ideas in nutrition science? If any species would be expected to be gluttonous and eat as much as possible of whatever the food provided, then voracious swarming locusts are it. But we knew that locusts are not so simple-minded—they can regulate their intake of nutrients, notably protein, even if that requires consuming their neighbors. What would the results of our big experiment show?
Before we find out, we first need to provide a short primer on nutrition.
CHAPTER 1 AT A GLANCE
1 We began our journey by describing an experiment on locusts, which pioneered a new approach to the study of nutrition.
2 We discovered that an appetite for protein is behind locusts’ reputation as plague-forming scourges of agriculture.
3 Will an appetite for protein play similarly important roles elsewhere in the animal kingdom? Even for us?
2
Calories and Nutrients
GIVEN THAT NUTRITION IS SO INFERNALLY complicated, let’s ask a simple question: Why must we eat?
Certainly, food today has become the source of a great deal of confusion and anxiety, which is a terrible pity because food is also the source of so much that is good—excellent, in fact. Food binds us together socially and culturally. It gives a great deal of pleasure while also providing the stuff that fuels life itself.
Energy is the most familiar of the things we need from food. Not a day goes by without seeing numbers written all over our foods, meals, and now also menus—like mathematical graffiti saying how much energy they contain and stern dietary guidelines warning how much of it we should eat. The labels don’t use the word energy, of course. You’re probably more familiar with the term Calories.