Future Humans: Inside the Science of Our Continuing Evolution 9780300224504

Citation preview

F U T U R E

H U M A N S

n e w

h a v e n

a n d

l o n d o n

Continuing Evolution

s c ot t

FUTURE HUMANS

Inside the Science of Our

s o lo m o n

Published with assistance from the foundation established in memory of James Wesley Cooper of the Class of 1865, Yale College. Copyright © 2016 by Scott Solomon. All rights reserved. This book may not be reproduced, in whole or in part, including illustrations, in any form (beyond that copying permitted by Sections 107 and 108 of the U.S. Copyright Law and except by reviewers for the public press), without written permission from the publishers. Yale University Press books may be purchased in quantity for educational, business, or promotional use. For information, please e-mail [email protected] (U.S. office) or [email protected] (U.K. office). Set in The Sans type by Integrated Publishing Solutions. Printed in the United States of America. Library of Congress Control Number: 2016936483 ISBN: 978-0-300-20871-9 (hardcover : alk. paper) A catalogue record for this book is available from the British Library. This paper meets the requirements of ANSI/NISO Z39.48-1992 (Permanence of Paper). 10 9 8 7 6 5 4 3 2 1

To my family— Past, present, and future

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Contents Introduction, 1 1.

Genomes and Germs, 13 2.

Big Data, 35 3.

World in Transition, 73 4.

Sex, 95 5.

Small Partners, 125 6.

Beyond the Horizon, 153 Epilogue, 179 Notes, 185

Acknowledgments, 213 Index, 217

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i n t r o d u c t i o n

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e humans are an odd species. I make that statement as someone who studies insects for a living, so I feel I have some perspective on strange critters. There are far more insects in the world than people, but humans are the only organisms that have come to dominate the Earth so completely. We have found ways to modify our environment to suit our needs, building climate-controlled spaces that allow us to live almost any­ where. We grow our own food, use chemicals to combat diseases, and propel ourselves in machines that allow us to move effortlessly from place to place. We have literally left a mark on our planet that is visible from space, which we know because we have been there and seen so for ourselves.

Yet our species has not always been so remarkable. Our an-

cestors from just 6 million years ago would, if they were alive today, be recognized as just another great ape much like the chimpanzees, gorillas, and orangutans that are still among us. In fact, living chimps can trace their lineage back to that same ancestor, but for whatever reason the intervening 6 million years did not result in nearly as much change for their lineage as it did for ours.

To get a sense of just how much has changed along the branch

of our family tree that led to the twig we call Homo sapiens, I visited 3

the David H. Koch Hall of Human Origins on the second floor of the Smithsonian’s National Museum of Natural History in Washington, D.C. The exhibit focused on some of the more notable milestones in our evolutionary past—walking upright on two legs, developing tools, growing substantially larger brains, harnessing fire, and developing language—characteristics we take for granted as quintessentially human but that are relatively recent developments.

Seeing such an exhibit also makes it clear how much we now

know about our past. Over the last century and a half, archeologists and paleoanthropologists have unearthed an incredible number of bones, tools, and other traces of our ancient ancestors. Many of these discoveries have occurred in just the last few decades. It doesn’t seem like that long ago I was a college student at the University of Illinois who became fascinated with the study of human evolution. I took every class I could find on the topic, and even considered pursuing it through a career in biological anthropology. Many of the fossils on display at the Smithsonian—fossils that have provided key insights into our evolutionary past—had not yet been described when I was an undergraduate in the 1990s.

In 1871 Charles Darwin wrote The Descent of Man and Selection

in Relation to Sex, a sequel to his book on evolution, already famous, in which he extended his theory about how species change through natural selection to argue that humans evolve, too.1 But the fossil evidence that would later support his claims was not yet available. The only fossils of a human ancestor that were known were the remains

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of Neanderthals (Homo neanderthalensis) discovered in Germany in 1856, which were decidedly more humanlike than apelike. Darwin predicted that additional and far more primitive hominids would be discovered, and he even went so far as to suggest they would be

true, although at first it seemed Darwin’s geographic speculation was pretty far off. In 1890, only twenty years after publication of The Descent of Man, Dutch anatomist and paleontologist Eugène Dubois erectus on the Indonesian island of Java.

Eventually, Darwin’s conjecture proved to be correct—the ear-

liest members of the human lineage, known as hominins, did indeed come from Africa. The first to be discovered on the African continent came from Zambia and then another, even older fossil was found in South Africa. Many more discoveries would follow. A wall of fossil skull replicas in the Smithsonian display made it clear at a glance just how many have since been found. It also showed how much has changed in our lineage even just from the neck up. Some skulls had thick eyebrow ridges and a bony crest running across the top, while others had a muzzle that looked more like the face of a chimpanzee. Some fossils had both chimplike and humanlike features. I took a close look at an artist’s full-body reconstruction of Lucy, the famous fossil skeleton of Australopithecus afarensis discovered in Ethiopia in 1974, and could clearly see that she had feet like ours but a small head, showing that the ability to walk on two feet evolved before a large brain.2

Our own species is relatively new, though our exact age is the

subject of much debate. The leading candidates for the first fossil Homo sapiens come mostly from Ethiopia, and radiometric dating of volcanic rocks near the fossils suggests that we had come into existence by about 160,000 years ago. By 50,000 years ago, the first Homo sapiens left Africa, following the trail blazed a million years earlier by our cousin, Homo erectus. We spread far and wide, and would eventually come to occupy nearly every corner of the globe.

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unearthed the fossilized remains of what is now recognized as Homo

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found in Africa. It did not take long for part of his prediction to come



That’s usually where the story of human evolution ends. We

evolved at some point in the past into modern people who eventually developed agriculture and civilization, and the rest, quite literally, is history. Looking at the skeletons on display at the museum, I could see how someone could assume that, biologically, we are the exact same people we were 150,000 years ago. Our bones certainly look the same. And it stands to reason that the evolutionary processes that shaped our ancestors no longer apply to us today. After all, many of us live in permanent structures with controlled climates that keep us separated from nature. We can wake up on one side of the planet and sleep that night on the opposite side. We use chemicals to sterilize our living spaces and our bodies. When we get injured or sick, we can have surgery to repair the damage or take drugs to eliminate the disease. If we have difficulty having children, we can make an embryo in a lab and have it implanted in the womb. We have created artificial limbs, hearing aids, and contact lenses. In today’s world, it hardly seems true that only the fittest survive.

Although there is general agreement among researchers that

humans evolved from chimpanzeelike ancestors, there has never been a scientific consensus on whether human evolution is still occurring. The philosophy of eugenics was created in the late nineteenth century (by Charles Darwin’s cousin Francis Galton) based on the misguided principle that our species is headed in the wrong evolutionary direction and that steps should thus be taken to intervene. Eugenics became a discipline unto itself, and although the term is today largely

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associated with racist and discriminatory practices, many leading scientists subscribed to its basic principles (which assumed that human evolution is ongoing) before the Second World War.

Support for eugenics waned following the global outrage

human evolution is continuing was still championed by a few key thinkers. In 1959, Theodosius Dobzhansky, one of the most influential ­twentieth-century biologists, delivered a lecture at Yale University to of On the Origin of Species. In his talk, which later became the book Mankind Evolving, Dobzhansky—while shunning eugenics—used the evidence available at the time to conclude that evolution continues to operate in humans, though he struggled to provide many examples.3

Not all of his colleagues agreed with his general premise of

continuing human evolution. In 1963, the eminent evolutionary biologist Ernst Mayr wrote, “We cannot escape the conclusion that man’s evolution toward manness suddenly came to a halt.” Though the topic is rarely discussed, Mayr’s view has largely persisted. It was echoed in 2000 by another highly regarded evolutionary thinker, Stephen Jay Gould, who said in an interview that “natural selection has almost become irrelevant in human evolution. There’s been no biological change in humans in 40,000 or 50,000 years.” In 2013, revered nature broadcaster David Attenborough echoed this idea when he suggested that “we are the only species to have put a halt to natural selection.”4

The trouble with this view is that evolution is constantly hap-

pening all around us. Any change in how common a trait, or the gene that codes for the trait, is from one generation to the next counts as evolution. We can see, watch, observe, detect, expect, and test for it, and—in some cases—predict its outcomes. Bacteria and fungi routinely evolve resistance to antibiotics. Viruses such as HIV evolve so quickly within their human hosts that the virus that may eventually

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mark the hundredth anniversary of Darwin’s landmark publication

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over the Nazi perversion of its principles. Yet, the basic idea that

cause death from AIDS is not the same virus that initiated the infection. The rapid evolution of viruses is what makes the development of vaccines against them so tricky—a virus is a moving target.

We can witness larger organisms evolving, too, but it requires

some patience. The larger the organism, the longer it takes to grow and begin to reproduce. Because evolution is by definition change that happens over generations, the longer the time between generations, the more slowly changes occur.

Nevertheless, in the 150-plus years since Darwin first intro-

duced the world to natural selection, biologists have noted many examples of it in action. In 1986, biologist John Endler published a monograph entitled Natural Selection in the Wild, in which he described the methods and challenges of studying evolution in nature.5 Chapter 5 of the monograph summarizes the studies that, by the mid-1980s, had documented natural selection occurring in wild populations (that is, not in a lab). It contains a table listing every such study of which he was aware that met his strict set of criteria. The table spans twenty-five pages. The species include complex organisms from across the tree of life—plants, mollusks, crustaceans, arachnids, insects, fish, amphibians, reptiles, birds, and mammals.

Making the leap from studying recent and ongoing evolution

in other species to studying it in humans has taken some time. But in the last several decades, research in a wide range of disciplines— paleoanthropology, molecular genetics, microbiology, evolutionary psychology, medicine, demography, and evolutionary biology, to

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name but a few—has brought new data to bear on the question of our continuing evolution. The practitioners of these disciplines do not always talk to one another, so the emerging conclusion—that our species never stopped evolving and that we are entering a new

interesting and less predictable than ever before—has gone largely unnoticed.

One biologist who has taken note of this phenomenon is

of Prometheus in which he made a strong case that human evolution has proceeded into modern times—and that it may in fact be accelerating—and backed it up with a lot of data.6 Wills provided an update of sorts for Dobzhansky’s case, citing numerous examples of natural selection operating in recent history and even in modern populations. Wills reminded us that natural selection is not the only way that evolution can happen. Other ways that genetically based traits can become more or less common over generations include the mixing of genes from one population to another through migration as well as random fluctuations that can happen when populations grow or shrink, all of which is relevant to modern humans. Wills’s evidence for continuing human evolution came primarily from data available by the late 1990s in the field of genetics. It was a discipline on the verge of a revolution that would confirm many of Wills’s tentative conclusions, force a reexamination of others, and provide more than a few surprises.

If human evolution is still occurring, how might the people of

the future be different from people living today? Imagining the future of our species has long provided rich subject matter for science fiction writers, beginning with H. G. Wells’s 1895 classic, The Time Machine, in which future humans evolve into two distinct types—Eloi and Morlocks.7 Wells’s Eloi have diminished physical and intellectual abilities because of generations of disuse, and are tended like livestock by the apelike, subterranean Morlocks. A similar theme of

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Christopher Wills. In 1998, Wills published a book entitled Children

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phase in our evolutionary history, one that makes the future more

disparity between coexisting but distinct types of humans underlies the X-Men comic books and films, in which so-called mutants possess superhuman abilities that are used first for their persecution but subsequently make them heroes. The 2008 Disney/Pixar film WALL-E depicted a future not unlike Wells’s original dystopia—humans, who have left Earth, have become overly reliant on technology, rendering them obese, unable to walk, and fully dependent on machines. Other popular films, from the Terminator series to The Matrix trilogy, have imagined our future as a struggle against our own technology.8

But that is science fiction. What about actual science? When

I reached the end of the Hall of Human Origins exhibit, I was delighted to find a touchscreen display with the words

future humans

that seemed like it might have some answers. I eagerly selected answers to a series of questions, but discovered it was an interactive game that presented hypothetical scenarios for the future (“Imagine all the land is underwater . . . will you have big webbed feet like a duck or long, stiltlike legs like a flamingo?”), meant to prompt visitors in thinking about how natural selection operates. I left the exhibit having learned a lot about our evolutionary past, but still wondering about our future.

The last part of the museum display, with its whimsical sce-

narios, seemed to reflect the attitudes of the many scientists who have been reluctant to give serious consideration to our evolutionary future. I was especially struck by this reluctance on the evening of

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October 10, 2011, when I attended a public lecture in Houston given by the famous British evolutionary biologist Richard Dawkins. Having spent much of my adult life studying, researching, and teaching evolution, seeing Dawkins speak in person was incredibly exciting. He was promoting his latest book, written for children, about the

works. When he finished his carefully prepared remarks, Dawkins opened the floor for questions. After a series of pointed remarks by audience members that seemed intent on drawing Dawkins into a in the aisle and asked a simple question: Are we still evolving, and if so, what are we evolving into? Dawkins replied that this is the single most common question he is asked, but that he refuses to answer it because to do so would require pure speculation.

On the one hand, as a fellow scientist I understood Dawkins’s

reluctance to speak on a subject for which he did not have empirical data. We are trained to be as objective as possible and to draw only the conclusions that are appropriate given the information available. Guesses, supposition, and so-called hand-waving interpretations of experimental results are not considered suitable activities for serious researchers. Dawkins was simply being a responsible scientist.

On the other hand, I felt there must be something that we can

say about the direction our species is headed. Do we really not know anything about the ways in which humans are still evolving? Has anyone looked for evidence of evolution in modern people? And if we are still evolving, is there really nothing we can say about which historical trends are likely to continue, and which seem more likely to be irrelevant in the modern—and future—world?

These questions became the basis for this book. To answer

them, I have read hundreds of research articles, attended seminars, spoken with the people doing the research—including anthropologists, biologists, geneticists, medical doctors, and psychologists— and visited their offices, labs, and field sites. My approach has been to ask these experts what they believe we can say about how our

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debate on religion, a young women stepped up to the microphone

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myriad explanations that humanity has invented for how the world

species is changing through natural selection and the other forces of evolution, and in what ways we are likely to continue to change in the future. Where appropriate, I have used what we know about evolution in other species to shed light on our own situation. This book is my attempt to explain what I have learned, making clear what predictions we can make—and what we cannot—about our evolutionary future.

As we will see, we live in an exciting time. We now know

more than ever about our biology and about our history, allowing us to peer into the future with greater clarity than has previously been possible. But at the same time, the changes we are undergoing, brought about by our own advances in technology, medicine, ­transportation—and by the growing impact we are having on the world around us—mean that we live in a time in which the future looks increasingly less like the past. We have become an odd species indeed, but our story is not yet over. Like all species, Homo sapiens continues to evolve, so there is one thing we can say with certainty:

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the people of tomorrow will not be the same as the people of today.

1 . Genomes and Germs

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J

une 26, 2000, was a big day for science. President Bill Clinton held a press conference in the East Room of the White House to make the announcement. He was joined via satellite by British prime minister Tony Blair and in person by two rival scientists, Francis Collins and J. Craig Venter, who represented two different approaches to tackling a major research objective—a detailed map of the human genome.

Collins was the U.S. government’s choice to

head a massive publicly funded effort to decipher the entire sequence of all human genetic mate-

rial. The Human Genome Project had begun in 1990 and included

researchers from twenty institutions spanning six nations. It was expected to take fifteen years to complete. Then biologist and entrepreneur J. Craig Venter announced in 1998 that he intended to do the same in only three years by forming a private company, Celera Geno­ mics, that would utilize a new, thus far unproven sequencing technique.

The ensuing competition has been described as the most fero-

cious in the history of modern science. In the end, both groups agreed to announce their results at the same time, and also to synchronize the timing of their formal research publications. The White House press conference indicated the scope of the accomplishment. In his remarks, President Clinton compared the first map of the human genome to the first map of North America created by the explorers Lewis and Clark, describing the genome draft as “the most important, most wondrous map ever produced by humankind.” News reports hailed it as akin to landing on the moon or splitting the atom.1 15



Most of the public attention surrounding the Human Genome

Project focused on its promise to revolutionize human health. But deciphering the human genome had other potential, too. A genome is the sum total of all genetic material—the full sequence of DNA of an individual—that together constitutes a sort of biochemical instruction manual for how to build and care for a living thing, whether it’s an oak tree, a butterfly, or a human. Amazingly, there is a complete genome inside nearly all of your cells.2 The DNA consists of long strings of nucleotide bases in parallel strands that are wound up tightly into packages called chromosomes, which direct the cell’s function from their sanctuary inside the nucleus. Each individual’s chromosomes come from his or her parents—half from the mother and half from the father—but not in identical form. As each sperm and egg is formed, the chromosomes inside them swap chunks, creating mosaics in which all of the original parts are still there but in a different order. This reshuffling creates new gene combinations that ensure no child is too much like either parent—despite what your spouse may say about how you’re turning into your mother or father.

Because a genome of a living species is inherited, it is also a

record of the history of its lineage. Think of a genome as a sort of ancient text that has been altered by each of its successive users to make it relevant for the current times and circumstances. The ma-

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jority of our genes date back to the Precambrian era some 600 million years ago, when all life consisted of single-celled organisms that lived in the sea.3 Many of these genes remain largely unaltered—in our cells as well as those of every other species—since their function is so absolutely essential to the basic operations of life. Examples include genes that direct the formation of the cytoskeleton that forms the structural foundation for cells and those that control cell division.

In general, any change to a DNA sequence that affects the

function of the gene it comprises should affect the organism one way or another. Mostly, the change will be for the worse. You simply

portant. This is why most mutations to functional genes are thought tions that swap one DNA base for another within genes cause some sort of reduction in survival or reproductive output.4

Though most of our genes predate the origin of complex life,

others we picked up and tweaked along the way, like genes that allow us to breathe oxygen or perceive light. We eventually gained versions of genes that control the formation of our bodies, with a head at one end and an anus, thankfully, at the other. Much later, we acquired genes that covered us in hair—until changes to those genes took much of that hair away. More recent acquisitions include gene variations that govern complex patterns of thought and reasoning as well as versions of genes that allow us to communicate those thoughts with one another through speech and symbols like the ones you are now reading.

Indeed, our bodies and our genes are a living testament to

the lives of our ancestors, and so the deciphering of the human genome promised to provide new insights into our evolutionary past. We could find out how, exactly, natural selection has operated and which genes it has affected. We could look for clues about what genetic changes make us different from our primate relatives, and when exactly we acquired them. We could piece together our history so much more thoroughly than would ever be possible with fossils and artifacts alone.

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to be harmful. Studies estimate that as many as 75 percent of muta-

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without messing something up. It will probably be something im-

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cannot tinker with something as intricate as the instructions for life

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The technology behind the sequencing of the human genome

advanced quickly toward the end of the twentieth century. As an undergraduate student at the University of Illinois in the mid-1990s, I worked in a research lab where, after first paying my dues by washing lab equipment, I was trained to sequence DNA. The method we used, first developed by British biochemist Fred Sanger in 1977, came to be known as Sanger’s chain termination method, which earned him his second Nobel Prize.5 Sanger’s method involved copying sections of the DNA molecules and pasting them into bacteria, which conveniently make lots of copies of themselves, and thus also the copied DNA, simply by growing in a petri dish. The large amounts of DNA they produce could then be isolated, purified, and sequenced.

Reading the DNA sequence was the trickiest part. I had to first

make a very thin gel by positioning two rectangular sheets of glass separated at the top by a thin piece of plastic and then carefully taping the other three sides to prevent leakage. I would then heat a gel solution in a microwave oven and pour it into the top of the rig, in much the same way as you might pour Jell-O into a mold, and then let it solidify as it cooled. Inevitably, a small air bubble would form somewhere in the gel, which I would carefully try to push toward the top; if I failed, that part of the gel could not be used.

The DNA molecules that had already undergone the chain

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termination procedure would then be injected with a syringelike pipette into narrow channels at the top of the gel, which was positioned upright with the top and bottom sitting in a vat of liquid so that an electrical current could pass through the entire apparatus. Because DNA is negatively charged, the fragments would be attracted to a positive charge at the base of the gel, forcing them to slowly pass through the gel. Smaller segments of DNA would travel

few hours, the DNA fragments had arranged themselves neatly according to size. Dunk the gel in a tub containing a radioactive isotope

to one of the four nucleotide bases (adenine, thymine, guanine, or bases by starting at the bottom of the gel and moving toward the top, recording which column contained a visible band. This was slow, tedious work, which of course is why you train undergrads to do it.

I began graduate school in 2000, the same year that the first

draft of a human genome was announced. By that time, machines were available that could perform an automated version of the Sanger sequencing process I had been doing manually. As a doctoral student, I was fortunate to join a lab at the University of Texas at Austin that had such a machine. Ours was an ABI 3100, known as a capillary sequencer because of the thin tubes that looked like plastic spaghetti strands that replaced the cumbersome gels I had been pouring by hand. Each of the narrow capillary tubes contained a gel that would separate DNA fragments by size and used fluorescent dyes that could be read by a laser rather than dangerous radio­ isotopes. The nucleotide sequence was recorded digitally and conveniently output to an attached computer.

Members of our lab treated the 3100 like a sacred object. It lived

in its own room, and its components had to be carefully cleaned before and after each use. But the extra care required was a small price to pay for the speed and efficiency with which DNA sequences could be generated on the 3100. It could run ninety-six samples at a time, each of which would read DNA fragments up to about a thousand nucleo-

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cytosine), my job was then to simply determine the sequence of

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glowing bands on an X-ray film. Because each column corresponded

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that would stick to the DNA, and the fragments would appear as

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slightly faster, so by the time I shut off the electrical switch after a

tides in length in less than a day. Anytime the 3100 was running, which was most of the time, we knew that our research was progressing.

Of course, even well-equipped individual university research

labs like the one of which I was a member in the early 2000s were tiny compared to the major research institutes working on the Human Genome Project. At these facilities, such as the Whitehead Institute / MIT Center for Genome Research or the U.K.’s Sanger Institute, dozens of these machines were operating simultaneously. An MIT news report in July 2000 boasted that “the [human genome] project consortium has been producing 1,000 bases per second of raw sequence–seven days a week, 24 hours a day.”6

The DNA sequencing technology available at the start of the

twenty-first century provided the raw material for making evolutionary insights from our genes. For the first time, there was an ­opportunity to look into the full length of the ancient text that is our genome and figure out how evolutionary forces like natural selection have tweaked it over millennia. What was still needed, however, were the proper statistical tools to extract the relevant information. ■ On the second floor of a new glass and steel high-rise at the Broad In-

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stitute in Cambridge, Massachusetts, Pardis Sabeti stood up in front of a packed room to introduce three researchers who worked under her supervision. She was petite, with long, dark hair and glasses, and she was wearing hiking socks but no shoes. She spoke quickly, giving an overview of the type of research her group was doing, which included genetic analyses of infectious diseases and their role in human evolution.

Apologizing to the group, which consisted of some of the most

highly regarded medical and population geneticists from across the northeastern United States, Sabeti explained she was very tired. It

by using all of the resources she and her collaborators had in place people had already died in Sierra Leone since the arrival of the virus in that country just a few months earlier, she explained. Many more were in hospital and showing worrying symptoms of the disease, which in the recent outbreak was killing four out of every five people showing up with symptoms. Some of the patients included nurses who had been caring for patients when they became infected, despite wearing protective gear. Sabeti was nearly in tears as she concluded her introduction, thanking all of her collaborators—some of whom had contracted Ebola and died.

Thirteen years earlier, Pardis Sabeti had been a graduate stu-

dent at Oxford University when she made a decision that would change her life. At the age of twenty-five, she was already a kind of academic superstar—she had been a National Merit Scholar at MIT, where she studied biology and from which she graduated with a perfect grade point average. She was first author on a peer-reviewed research publication before a Rhodes Scholarship brought her to Oxford for graduate training. Her academic career had not always been certain, though. When she was two, Sabeti’s family fled from Iran, where her father had worked for the shah’s government prior to the 1979 revolution. They were granted refugee status in the United States, where her extended family remained in hiding for several years, constantly moving from state to state. As a young girl, she was

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in Sierra Leone as well as back home in Cambridge. Nearly two hundred

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Africa was keeping her working around the clock in an effort to help

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was mid-July 2014, and an outbreak of the deadly Ebola virus in West

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enamored by nature and animals, imagining that one day she might become a veterinarian or perhaps a florist.

But as the child of a revolution, she understood the importance

of a stable job and so, taking advantage of her skills in mathematics, she set out to become a doctor. Becoming a Rhodes Scholar added an interesting twist to her education, though, and Sabeti found herself wondering how best to spend the two to three years she had been granted at the prestigious British university. Biological anthropologist Ryk Ward quickly noticed her, and he convinced her to pursue a doctorate in evolutionary genetics. Under Ward’s supervision, Sabeti decided to focus her attention on the role that malaria has played in human evolution by looking for signs that the deadly disease has left some detectable trace in the human genome.

Sabeti examined sections of DNA from people with and with-

out natural resistance to malaria. She began to notice a pattern— DNA from people with resistance had less diversity in the region surrounding the genes she was examining than did people without resistance. Sabeti thought this difference might have something to do with how long that particular section of DNA had existed, which might be a clue about its evolutionary history.

Her hunch was based on how DNA from different parts of

chromosomes gets swapped each time a sperm or egg cell is pro-

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duced. The result is that, as you look along any particular part of a chromosome, there is usually a lot of diversity. The pattern she was seeing among people with resistance to malaria suggested that there had not been much time for swapping to occur, implying that the sequence of DNA was relatively new. That the low variability sequence was present in numerous individuals who all had natural malaria resistance suggested that it was somehow tied to prevent-

several generations as a result of natural selection.

In a sense, natural selection just happens. In any population,

end up contributing the most genes to the next generation, so those mon. Any genes that directly or indirectly lead to the production of more offspring are said to be favored by natural selection. If a particular trait—like resistance to malaria—is favored by natural selection for many successive generations, the population will become better adapted to the local circumstances because more individuals will have the beneficial trait.

Sabeti came up with a mathematical model to describe the

pattern she was observing in the DNA sequence data, which gave her a way of looking for other parts of the genome with a similar profile. It worked—Sabeti’s method, known as the long-range haplotype test, pointed to two different genes that seemed to have experienced recent natural selection in response to malaria.7 In both cases, older tests that had been developed to look for signs of natural selection having operated deeper in the past were not able to detect it, giving further support to the idea that natural selection for these gene variants had happened recently. ■ The idea that malaria might be important for recent human evolution dates back to the middle of the twentieth century, in particular the year 1949, when a recent college graduate named Anthony Clifford Allison was collecting blood samples in Kenya.8 Allison was born

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genes—and the traits they encode—end up becoming more com-

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spring than others. The individuals that leave the most offspring

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some individuals will, for one reason or another, have more off-

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ing malaria infections and that it had become more common over

in South Africa but grew up in Kenya on a farm overlooking the Great Rift Valley. As a child he developed a fascination with nature and anthropology. Meeting the famous paleoanthropologist Louis Leakey when he was excavating nearby and later reading Darwin convinced Allison to explore his interest in human evolution and genetics. He went to college in South Africa and then medical school at Oxford, where, in 1949, he signed up for a research expedition that would bring him back to his childhood home.

While many of his colleagues were sampling plants and insects

in the central highlands of Kenya, Allison collected human blood samples from across the country. He noticed that the frequency of a blood trait known as sickle cell varied between indigenous populations.9 In low-lying areas near the coast and along the shores of Lake Victoria, more than 20 percent of the population had the sickle-cell trait, whereas in higher-elevation regions the frequency dropped to less than 1 percent. The pattern did not correspond to cultural or linguistic differences, but Allison noted that it did correlate with the prevalence of malaria.

Unlike normal red blood cells, which look like rounded discs

with dimples poked into each side, the red blood cells of people with sickle-cell disease are crescent shaped with pointed tips. The condition had first been described from an African American man in Chi-

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cago, and later work had revealed it was present in around 8 percent of the African American population. Allison’s discovery that as many as one in five people in some parts of Kenya have the sickle-cell trait was surprising given that the most severe form of the condition is often deadly.

The same year Allison was collecting blood samples in Kenya,

two published studies reported that sickle-cell disease was herita-

for sickle cell codes for the protein hemoglobin that contains iron and gives red blood cells their color. Hemoglobin is the protein that

DNA nucleotide to change from an adenine to a thymine results in a inherit one copy of each gene from our mother and one from our father, each person’s genome has two versions, or alleles, of any given gene. Sometimes the alleles passed down from Mom and Dad will be identical, but they can also be different. Having two alleles for sickle cell results in the life-threatening condition known as ­sickle-cell anemia. Having one sickle-cell allele and one normal hemoglobin allele means that a person does not suffer from full-blown sickle-cell ­anemia but may develop symptoms under certain circumstances that reduce oxygen levels, like intense physical exertion.

Allison speculated that people with a single copy of the

­sickle-cell allele, known to geneticists as heterozygotes, might have some resistance to malaria, but it would take several more years for his hypothesis to be confirmed.10 Allison returned to Kenya to conduct experimental work, taking advantage of studies by a pharmaceutical company that was testing malaria treatments by infecting volunteers with Plasmodium falciparum, the parasite that causes the deadliest form of the disease. The parasites normally enter the blood through the bites of mosquitoes, making their way first to the liver and later to the red blood cells, where they rapidly reproduce and burst forth from the cells, causing fever. He found that the blood of sickle-cell heterozygotes had lower levels of P. falciparum than others in the trial. It wasn’t a perfect experiment, though, since the volun-

2 5

change in the hemoglobin structure that leads to sickling. Since we

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transport it throughout the body. A mutation that causes just one

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binds to oxygen, allowing us to harness it from the atmosphere and

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ble. Subsequent work would establish that the gene responsible

teers were adults who had probably been exposed to malaria as children and may have developed some immunity to it. To test whether heterozygotes had lower natural rates of P. falciparum infection, Allison traveled to Uganda and accompanied a government health-care worker to a weekly market where he obtained blood samples from local children. Indeed, he found that children heterozygous for sickle cell had lower parasite counts and, perhaps more important, were far less likely to have very high levels of P. falciparum infection.

Subsequent studies found additional support for Allison’s hy-

pothesis, and the correlation between sickle cell and the historical prevalence of malaria was found to extend across all of sub-Saharan Africa as well as the Mediterranean, Middle East, and tropical Asia. It seemed that in places where malaria caused by P. falciparum was historically common, people with one copy of the sickle-cell allele left more descendants than people with either zero copies or two copies. In fact, children in such regions who were heterozygous for sickle cell were estimated to be 26 percent more likely to survive into adulthood than children with two normal hemoglobin alleles. This became the first well-established example of how a harmful hereditary disorder could be maintained in a population because it was advantageous to be heterozygous—and also provided evidence that natural selection was still operating in twentieth-century human

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populations.11

Malaria continues to play a role in human evolution because

of how common—and how deadly—it is, especially for young children and pregnant women. Despite the development of drugs to both prevent and treat infections, there are nearly 200 million cases of malaria worldwide each year, resulting in approximately 600,000

on average one child dies each minute from the disease.

In such regions, natural selection favors any condition, like

its host, many of the traits favored by natural selection affect blood One such example is thalassemia, a set of conditions that also affect hemoglobin. Likewise, deficiency in a protein known as G6PD, which plays an important role in detoxifying red blood cells, is also known to provide natural resistance to malaria.13 It was the gene for G6PD that Pardis Sabeti used as the first test case for her new method to detect selection in the genome. ■ After finishing her dissertation on the role of malaria as an agent of natural selection in humans, Sabeti returned to the United States to study medicine at Harvard Medical School, where she became only the third woman ever to graduate summa cum laude. In 2008 she became an assistant professor at Harvard and began building a lab group with a focus on the impact of infectious diseases on recent human evolution. Her group developed a new test for detecting selection in genome data that built on her original long-range haplotype test and also incorporated tests developed by others. Applying it to genome data from the Yoruba people of West Africa, Sabeti and her colleagues found that the top candidate for a region of the genome under selection was a gene called LARGE. Normally, LARGE affects the ability of cells to interact with their environments, but

2 7

cells, making them a less hospitable environment for the parasite.

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Because Plasmodium must reproduce inside the red blood cells of

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sickle cell, that interferes with the Plasmodium parasite’s life cycle.

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annual deaths.12 The disease remains most common in Africa, where

it was also known to regulate the ability of a deadly virus to enter human cells.14

The virus in question causes a pernicious disease known as Lassa

hemorrhagic fever that is endemic to West Africa. In some countries, one in every five people had been exposed to the virus and, although it was implicated in thousands of annual deaths, as many as 90 percent of West Africans exposed to the virus never developed symptoms of the disease. In collaboration with researchers in Nigeria, Sabeti identified several parts of the Yoruban genome that fit the profile of having responded to natural selection for resistance to Lassa fever. Their data suggested that in regions where Lassa is endemic, people with the resistance alleles are more likely to live longer and hence have more opportunities to have children than those who do not.15

The project expanded to Sierra Leone, where a local doctor,

Sheik Umar Khan, had established a special ward at Kenema Government Hospital that focused specifically on diagnosing and treating patients with Lassa fever. But their work on Lassa was interrupted on May 25, 2014, when the team working at the Lassa clinic documented the first case of Ebola virus in Sierra Leone. The disease had apparently crossed the border from the neighboring country of Guinea, where the West African Ebola epidemic had begun several months earlier. The team immediately put their Lassa work aside to help with

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the crisis.16 In addition to doing what they could to provide supplies and raise international awareness of what was happening, the team collected samples from patients admitted to the Kenema Government Hospital Lassa ward. They used their onsite technology to diagnose new Ebola cases and also brought samples back to Sabeti’s lab in Cambridge to sequence the virus’s genome, racing to provide what information they could about the unfolding outbreak.

On August 28, 2014, Sabeti and her colleagues published their

initial analysis of ninety-nine Ebola genomes the team had collected from seventy-eight different people, allowing them to trace in de-

dred deaths in that country alone, and hundreds more in the region. including Dr. Khan, who had led Sierra Leone’s efforts to combat Lassa and then Ebola—had contracted the virus and died.

Sadly, the outbreak was only just beginning. By mid-­September,

the infection rate was accelerating, with 562 Ebola-related deaths in Sierra Leone, and some 2,500 in all three affected West African nations combined. On September 18, the United Nations Security Council declared the epidemic a “threat to international peace and security.” The next day, Thomas Eric Duncan boarded a flight from Liberia to Brussels and then another to the United States. Several days after arriving in Dallas, he developed a fever and began vomiting. He was eventually admitted to a hospital, where he later died. Two of the nurses who treated him became infected but survived. In Spain, a nurse treating two missionaries who contracted Ebola in West Africa became infected. The nurse lived; both missionaries died. By the end of 2014, the global death toll was approaching 8,000. One year later, the outbreak finally came to an end—after more than 28,600 cases and 11,316 deaths.18 ■ Scanning human genomes for signs of natural selection is still a fairly new approach, but the techniques developed by Sabeti and others suggest that infectious diseases have been among the most

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By the time their paper was published, five of Sabeti’s coauthors—­

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outbreak in Sierra Leone had already resulted in more than two hun-

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tail the history of the outbreak and pinpoint its likely origin.17 The

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important influences on our evolutionary history. Some of the diseases affecting us today are old adversaries that have been with us for millennia. Malaria, for instance, has probably been infecting and killing humans since at least the origin of our species about 160,000 years ago.19 Other infectious diseases were acquired as we left Africa around 50,000 years ago, as people encountered environments—not only climates, plants, and animals but also microorganisms—never before seen in our evolutionary history.

The development of agriculture and the domestication of an-

imals had a twofold effect. They caused an increase in population densities that made it easier to spread diseases while also exposing people to microbes that had previously been found only in the wild ancestors of the animals that were domesticated. Indeed, the majority of modern infectious diseases—around 60 percent—are the result of a virus, bacteria, fungus, or protozoan that switched from infecting an animal to infecting humans.20 We acquired anthrax from sheep and cattle; influenza from birds, pigs, and horses; rabies from dogs—and there are about two hundred other microbes that crossed species lines and began infecting people.

Many of these zoonotic diseases, as infections acquired from

animals are called, are scourges our species has battled for the last ten thousand years or so. Some, like the bubonic plague and influ-

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30

enza, have caused periodic outbreaks that resulted in the deaths of a significant proportion of the human populations in which they emerged. Others, like tuberculosis, which has an even longer history of infecting us, have been a near-constant presence. Not surprisingly, these diseases have impacted the rates of survival and reproduction for many generations, and natural selection has led to a range of dif-

like Pardis Sabeti are only beginning to uncover.21

But other infectious diseases, including Ebola and HIV, are

cause there are so many of us—the global population is projected have to continually find new hosts in order to survive. Since 1940, about four hundred new diseases have begun infecting humans.22 As our population grows, we will become an even bigger target for emerging infectious diseases. We are also social creatures who interact with one another, passing microbes as we do. What’s more, our technology allows us to move around the globe better than any other large organism on Earth, meaning that our ability to spread disease is unmatched. Whereas the deadly influenza pandemic that began in 1918 took three years to spread around the world, an outbreak of a new strain of influenza known as H1N1 in 2009 reached four different continents in just three weeks traveling along international airline routes.23

The take-home message is that we are entering an era in

which we face a near-constant barrage of new infectious diseases. The extent to which they will act as agents of natural selection, as they have done throughout history, will depend in part on how those diseases affect our survival and reproduction. For people living in more developed regions, infectious diseases are no longer the leading causes of death. Vaccination and antibiotics, along with other medical advances and improvements in sanitation, led to the near elimination of diseases such as smallpox, diphtheria, and tuberculo-

31

to reach 9 billion by 2050—we are a prime target for diseases, which

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switching hosts, and sometimes those new hosts are humans. Be-

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relatively new. Viruses, bacteria, and other microbes are constantly

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ferent evolutionary adaptations to combat them that researchers

sis in Western nations in the twentieth century. Infectious diseases have been replaced by noncommunicable conditions, including cardiovascular disease, cancer, and diabetes, which are now the most common causes of death in more developed regions.24

But most of the world’s population—about 83 percent—lives

in less-developed regions, where infectious diseases remain a major problem. Lower respiratory infections, HIV/AIDS, and diarrheal diseases are the leading causes of mortality in such areas where, combined with malaria and tuberculosis, they are responsible for about one-third of all deaths.25 Fully 40 percent of deaths in less developed regions occur among children under the age of fifteen, whereas the same age group makes up only 1 percent of deaths in more developed regions. Because these diseases cause so many deaths, especially among children, natural selection continues to favor any natural resistance to them.

Making matters worse, many of our go-to weapons in the war on

germs are quickly losing their effectiveness. We have unwittingly entered into an arms race with enemies that have an inherent advantage. Antibiotic resistance evolves in bacteria—such as ­methicillin-resistant Staphylococcus aureus, or MRSA, a dangerous and increasingly common source of infection—as the result of strong natural selection imposed by our use of antibiotics. Microbes have an advantage be-

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cause they can evolve resistance far faster than we can develop new drugs, thanks to their short generation times, which can be as little as thirty minutes.26 In the span of a week, bacteria such as MRSA can undergo about as many generations as humans have since the development of agriculture. We simply cannot keep up.

As we continue deciphering the ancient text that is the human

genome, one of the principal messages coming into focus is this: the

than just an occasional blight or a passing nuisance. Infectious diseases have been among the most important drivers of our evolution-

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major role in our species’ future.

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ary past, and there is every reason to believe that they will play a

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microscopic organisms that cause us to become sick have been more

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2 . Big Data

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T

he unassuming city of Leicester, located in the Midlands region of En­ gland about a hundred miles north

of London, was an important place for the origin of evolutionary biology. In 1844, at the library of the Mechanics’ Institute on Wellington Street, a young schoolteacher named Alfred Russel Wallace met another young man by the name of Henry Walter Bates. Both had in interest in natural

history—Bates was an avid collector of butterflies and beetles, and Wallace had a love of botany. Bates introduced Wallace to the incredible diversity of insects that could be collected nearby, and the pair began making small collecting trips together in the English countryside. A few years later, in 1848, they embarked together on a much more ambitious expedition—to the Amazon rainforests of Brazil. Wallace would remain there for four years before returning home, narrowly escaping death when his ship sank, taking with it many of his precious specimens. Before long, though, he was off again to another exotic tropical locality, this time the islands of the Malay Archipelago in Southeast Asia.1

Wallace continued making extensive zoological collections,

which he sold in England to make a living. His observations about the specimens he collected inspired him to develop a theory about how species change through time. Though he had been pondering the basic premise since his early days back in England, the critical 37

insight came to him rather suddenly while suffering from a malaria-induced fever on the island of Ternate. In collecting numerous examples of the same species in different locations, both in South America and Southeast Asia, Wallace noticed subtle physical differences among individuals. Perhaps, he thought, those differences might somehow affect their ability to survive and reproduce, making some forms more likely than others to persist over generations. If so, this could explain how species gradually change, with populations in different places diverging as they accumulate different traits.

Eager to see if his theory would hold up to serious scientific

scrutiny, he wrote a letter explaining his idea to Charles Darwin, whom Wallace knew only by reputation. When Darwin read the letter, he quickly recognized that the obscure collector had independently come up with the same theory on which he had been working for nearly two decades—a theory of evolution by natural selection. Like Wallace, Darwin had arrived at the idea through careful observations of numerous specimens collected in distant parts of the world. Unlike Wallace, however, Darwin had been working diligently on the details of his theory for years, conducting experiments and seeking examples to illustrate the concepts he planned, eventually, to unveil.2

The letter from Wallace prompted Darwin to act sooner than

he might have liked. In an attempt to acknowledge Wallace’s insight without getting scooped, Darwin had a colleague present the idea to the prestigious Linnaean Society as a joint paper by both men.

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The following year, Darwin published a more complete explanation of the theory along with the evidence he had accumulated for it in a book entitled On the Origin of Species by Means of Natural Selec-

fathers.

A few miles from the library in Leicester where Wallace first met Bates, many of the top researchers in the field of human evolutionary genetics gathered in April 2014 to debate and discuss the many insights that genomics has given us about our evolutionary past. During seminars, and afterward over coffee or beer, the researchers swapped ideas about the latest DNA genotyping techniques, statistical methods for analyzing genome data, and what it all meant for the history of our species.

The field had come a long way, and it was now possible to

address questions about our evolutionary past that Wallace and Darwin could never have imagined. The completion of the Human Genome Project marked the dawn of what became known as the postgenomic era—but the sequencing of a single human genome was just the beginning. DNA sequencing technology accelerated in the 2000s at a rate that surpassed even the celebrated exponential growth in computing technology.3 The result has been what one of the conference organizers described as a data tsunami, with some 250,000 whole human genomes sequenced as of 2015—and the pace continues to accelerate rapidly. Such immense quantities of information, which has come to be known as big data, cannot be stored or analyzed using traditional methods. Indeed, the amount of genomic information produced each day is doubling every seven months, putting it on pace to surpass the current leader in production of big data, the social media site YouTube.4 By 2025, we may

39

■

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to a much lesser extent, Wallace—acknowledged as its founding

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tion. The field of evolutionary biology was born, with Darwin—and,

have sequenced as many as 2 billion individual human genomes, or about one-quarter of the projected global population.

Part of this acceleration is attributable to a decline in costs as

sequencing technology improves. Ewan Birney of the European Bioinformatics Institute pointed out to the conference attendees that the cost of sequencing an entire human genome in 2003 was about the price of the most expensive house in London. Ten years later, the same genome could be sequenced for about the cost of a family season ticket to watch the local soccer team. Birney predicted that, in five years, the cost will decline to about the price of buying dinner for that same family.

The other factor is the development of new types of sequenc-

ing technology. Sanger sequencing—the kind I learned to perform as an undergraduate and the method used to generate the first human genomes—has been largely replaced by so-called next-generation sequencing, which began in 2005. The major breakthrough was a shotgun approach in which the DNA is fragmented into small pieces that can be read simultaneously rather than one after another. Soon, a variety of next-generation sequencing methods became available, and both the time and price required to sequence a genome began to plummet. A representative from one of the leading producers of next-generation sequencing machines proudly announced at the conference that a much-anticipated technological achievement— the ability to sequence an entire human genome for just $1,000— had finally been accomplished.

The ability to cheaply sequence entire genomes made it pos-

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sible for the first time to sequence many of them and thus to be able to look at human genetic diversity on a large scale. Several such projects were launched in the 2000s, including HapMap, Genographic,

and cultural diversity.5

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lected from people representing a wide range of ethnic, linguistic,

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and 1,000 Genomes projects, in which genomic information was col-

One of the outcomes of these projects was the somewhat

counterintuitive conclusion that, as a species, humans are not very genetically diverse. This was somewhat surprising because, generally speaking, larger populations tend to contain more diversity than smaller populations because any individual can develop a mutation, contributing something new to the gene pool. At 7 billion strong, one might imagine that Homo sapiens would be especially rich in genetic diversity, but in fact we have less diversity in our genomes than do many of our closest primate relatives.

In a presentation at the Leicester conference, Spanish evolu-

tionary geneticist Tomas Marques-Bonet made this fact clear by contrasting human genome diversity with that of the other great apes. By comparing the number of single nucleotide polymorphisms—sites in the genome that differ between individuals by just one nucleotide base, such as an adenine instead of a cytosine—Marques-Bonet and his colleagues found that humans rank as among the least diverse apes. Several populations of chimpanzees, western lowland gorillas, and especially orangutans all have far more genetic diversity than we do—despite having population sizes more than ten thousand times smaller than our own.6 In fact, the number of single nucleotide polymorphisms discovered by sequencing just seventy-nine great ape genomes was more than twice the number found in more than one thousand human genomes.

The apes have high genetic diversity despite low population

sizes, researchers believe, because their populations used to be larger but have recently declined. Some populations, such as that of

western chimpanzees in the Ivory Coast, are estimated to have plummeted by as much as 75 percent in just two decades, largely because of habitat loss and poaching. Ongoing threats to their already small population sizes means that the great ape species are all now considered either endangered or critically endangered.7

With humans, the opposite is true—our populations were

once small but have grown exponentially. Graphical representations of the estimated global human population size over the last several thousand years show a classic J-shaped curve. Beginning at year AD 1, when there were fewer than 2 million people, the human population took about 1,200 years to double in size. But then it doubled again in just 500 years, then again in just 150 years, then 70 years, then—from 1960 to 1999—just 39 years. In 2016, the global population stands at over 7 billion and is projected to reach 9 billion by 2050.8

Human genetic diversity also differs depending on which pop-

ulations are sampled, as British geneticist Richard Durban reminded the Leicester conference participants. The HapMap and 1,000 Genomes data showed that the greatest amount of human genetic diversity exists among Africans, and that, as a general rule, the further a population is from Africa the less diversity it contains. This pattern matches archeological evidence suggesting that Homo sapiens left Africa around fifty thousand years ago and spread across the Middle East and into Europe, Asia, and Australia, eventually reaching the Americas and the remote Pacific Islands.

These explorers were venturing into terra incognita, facing

new environments and unforeseen obstacles. Natural selection

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helped populations to become better adapted to their surroundings, including new infectious diseases they faced in each region. As we spread, the leading edge of the human expansion would likely

ably not successful and left no descendants. Those who survived,

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however, established new populations that grew in size, and some of

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game to hunt or escaping from enemies. Many settlers were prob-

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have been just a small group of settlers, perhaps looking for new

their descendants would go on to found new populations, and so on. Geneticists describe this as a serial bottleneck pattern, and it leaves a characteristic signature in the genome. Each new population is a subset of the previous one, with diversity becoming progressively lower in each new settlement. By the time people reached the southern edge of South America, they had brought with them just a small fraction of the genetic diversity that was originally present back in Africa.

Genetic diversity is critical to evolution because it is the raw ma-

terial for natural selection. The more diversity a population has, the more potential there is for it to respond to natural selection; without any diversity to work with, as an evolutionary force selection becomes impotent. The size of a population is important because it usually correlates with genetic diversity but, as illustrated by the example of humans and great apes, the correlation is not always perfect. Population sizes, however, are relevant for another reason—they are related to another force of evolutionary change, one that is somewhat mysterious, often misunderstood, and probably responsible for shaping much of the genomic diversity present in our species today. Yet it took nearly one hundred years after Darwin’s and Wallace’s discovery of natural selection for biologists to recognize its importance. ■ As a teenager in Japan during the Second World War, Motoo Kimura discovered a connection between his two favorite school subjects—

botany and mathematics.9 His love of plants came from his father, a businessman with a passion for flowers. Mathematics was an interest young Kimura would develop on his own after reading geometry books while forced to stay home from school following a serious bout of food poisoning that killed one of his younger brothers. A high school course on the use of statistics in biology taught by a botanist demonstrated to Kimura that it was possible to pursue both of his passions simultaneously.

Kimura moved to the United States in 1953, traveling on the

only Japanese passenger ship to survive the Second World War, to enroll as a graduate student at Iowa State College. He would soon transfer to the University of Wisconsin, where he would be close to one of his heroes, the great population geneticist Sewall Wright. With Ronald Fisher and J. B. S. Haldane, Wright had founded the field of population genetics, which built upon the discovery of the genetic mechanism of inheritance and would be combined with Wallace’s and Darwin’s theory to lay the foundations for the modern discipline of evolutionary biology.

As a graduate student, Kimura delivered a presentation at the

1955 Cold Spring Harbor Symposium on Population Genetics to an audience that included many of the leading biologists of the day, including his hero, Sewall Wright, as well as Theodosius Dobzhansky and Ernst Mayr. At the same meeting the previous year, Anthony Allison had presented his evidence for the protection that the sickle-cell trait provides against malaria. The year before that (1953), James Watson and Francis Crick presented their model for the structure of

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DNA. Needless to say, these meetings were important.

According to his doctoral supervisor, who was also in atten­

dance, Kimura’s Cold Spring Harbor presentation was difficult to un-

ing, Wright stood up and congratulated Kimura on a “great accom-

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plishment.” For the young population geneticist who had always

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thick Japanese accent.10 Nevertheless, when Kimura finished speak-

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derstand because of both its mathematical complexity and Kimura’s

admired Wright’s work, this must have been something like having LeBron James compliment your jump shot.

But Kimura would soon present an idea that would result in

his name becoming nearly as well known among evolutionary biologists as his heroes Wright, Haldane, and Fisher. Writing in the journal Nature, Kimura used a mathematical argument to show that mutations appear at a higher rate in mammals than is expected from theoretical predictions.11 This could only be explained, he concluded, if most mutations that arise are not affected by natural selection because they do not have a noticeable effect on the survival or reproduction of the organism. Kimura was suggesting that another mechanism, called genetic drift, was actually among the dominant evolutionary forces influencing DNA.

The concept of genetic drift was not new. Sewall Wright him-

self had first described it in 1931, but before publication of Kimura’s paper in 1968, most experts, including Wright, saw drift as important mainly for very small populations.12 In most situations, natural selection was still seen as the primary agent of evolutionary change.

Kimura’s neutral theory of molecular evolution created quite

a stir among his colleagues, and Kimura would end up spending much of the rest of his life defending it. Debates about which force has more importance in human evolution—drift or selection—were common over beers outside the conference center in Leicester. Yet the basic premise Kimura put forth has become the default assumption against which any molecular data must now be tested—genes

are assumed to evolve neutrally unless the data can convincingly show that they are under selection.

The tricky thing about genetic drift is that its effects are

random, which makes it unpredictable. The role of chance is exaggerated in small populations, meaning that drift can have an even greater influence than natural selection, as Wright had argued. Those ancient human pioneers exploring new territories were subject to the whims of genetic drift because there were so few of them. By chance, the handful of people who became the founders of new populations would have had combinations of genes that were different than some of their kin back home. Some of those gene combinations became more common once the new population grew—not because they were better suited to the environment but simply because they happened to be present in the genomes of the founders. If you think of the edge of the expanding human population as a wave moving across the landscape, those gene combinations becoming more common in the people on the wave front gave rise to what population geneticists call gene surfing.13

Many of the genes common in modern human populations

may be surfers. A troubling realization for human evolutionary geneticists was that population size fluctuations that lead to drift and surfing can leave a signature in the genome that looks an awful lot like the signature of natural selection.14 Even in large populations like ours, gene variants that happen to occur in families that leave more descendants for reasons unrelated to the function of those genes will become more common due to drift. Tests like those developed by

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Pardis Sabeti to detect parts of the genome that have experienced selection initially turned up a large number of genes that are more common in one human population than another. Although some of

were at least as likely to have been caused by random drift.

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47

selection, more careful analyses have in some cases shown that they

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these seemed like good candidates for genes that have been under

One such case was the tantalizing publication in Septem-

ber 2005 of two papers that reported genes involved in regulating brain size that appeared to be under recent selection.15 The genes in ­question—called microcephalin and ASPM—are involved in a disorder called microcephaly, in which the brain does not grow to normal size, leading to intellectual disabilities. Given that the human brain is so much larger than the brains of chimpanzees and other apes, researchers looked for genes that might have been involved in the expansion of the brain in our ancestors, and microcephalin and ASPM seemed likely candidates as genes linked to brain size. When the scientists compared the sequences of those genes in humans, apes, and monkeys, the human sequences showed signals consistent with natural selection, and particular versions of the genes were found to be more common in some human populations—especially ­Europeans— than in others. They used a mathematical population genetic model to estimate the age of the particular versions of microcephalin and ASPM that varied among populations, and found them to be surprisingly recent—thirty-seven thousand and fifty-eight hundred years, respectively. The young age and population level differences led the authors to conclude that these genes must have experienced natural selection favoring larger brain sizes.

Unfortunately, the authors failed to eliminate all possible ways

that drift and demographic history—how the populations were structured geographically and how they expanded and contracted through time—could explain their data. What’s more, subsequent analyses by other researchers using other techniques could not find

any evidence for selection, suggesting that demographics and drift are more likely culprits. It was also unfortunate that the original publications, although they never said so explicitly, seemed to imply that microcephalin and ASPM had something to do with intelligence and that recent and ongoing selection had therefore led to differences in average intelligence between Europeans and Africans. Subsequent studies have found no evidence for any link between these genes and intelligence.16

Such false starts are typical of science, especially in fast-­

moving fields like evolutionary genetics. Attempts to understand the evolution of the human brain from a genetic perspective have been especially tricky, but there have been some other promising leads. For example, we now know that after we humans diverged from our common ancestor with chimpanzees, a gene known as SRGAP2 underwent a series of duplications. Think of it as copying a gene and pasting the copy in a new location within the genome. These copies now make proteins that interact with one another during brain formation, causing neurons in the human brain to be denser and to develop more extensive connections than in other species—possibly leading to enhanced cognitive abilities. Another interesting prospect is the gene FOXP2, which in humans affects speech but is also present in apes and other mammals. It makes an identical protein in Homo sapiens and our extinct relatives, the Neanderthals and Denisovans. But in chimpanzees, the same gene has a slightly different sequence, resulting in a protein with two amino acids that differ from the human version. These differences,

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combined with a pattern of DNA changes consistent with natural selection but not with genetic drift or surfing, suggest that FOXP2 may have been involved in the evolution of our unique language

Though future research will likely shed more light on the re-

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cent and continuing evolution of our brains, we know a lot more

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involved.17

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abilities, though many other genes are also thought to have been

about how natural selection has shaped other parts of our bodies. Take, for instance, our skin. Skin color varies widely among human populations, but not in a random way. Prior to the reshuffling of people around the world that began a few hundred years ago with the rise of intercontinental transportation and continues today, there was a close correlation between the global variation in human skin color and the intensity of ultraviolet light that reaches the Earth’s surface. Anthropologist Nina Jablonski has investigated this correlation extensively and believes it is no coincidence. Skin color, she has argued, evolved as the result of a compromise between two conflicting needs that both relate to ultraviolet radiation from sunlight and the ability to make a baby.18

Too much ultraviolet light is dangerous. Sunburn and skin can-

cer are just two of the more apparent ways that excess exposure to the sun can be harmful. Compared with our relatives the apes, humans have noticeably less hair covering our bodies, thereby increasing the amount of skin exposed directly to sunlight. Why we lost our body hair is a question anthropologists love to debate, but one of the consequences of becoming a naked ape was that our ancestors needed a new way to protect themselves from excess ultraviolet light, which is especially intense in the lowland tropics where our species originated.19

One solution was to use a naturally produced pigment called

melanin. Melanin acts as a natural sunscreen, absorbing and reflecting ultraviolet radiation, and is produced by a wide range of organ-

isms. In humans, melanin is made by skin cells near the base of the epidermis called melanocytes that stuff the newly made pigment into little packets called melanosomes and then ship them next door to another type of epidermal cell, keratinocytes, where they remain. All people have about the same number of melanocytes, but the melanocytes in individuals with darker skin make more of a darker version of melanin known as eumelanin. Their melanosomes are also larger and more evenly spread throughout the keratinocytes. The result is a very effective form of natural protection from ultraviolet radiation, equivalent to sunscreen with an SPF of 10–15 in people with the darkest skin.

The melanin in our ancestors’ skin would have helped to pre-

vent sunburn and skin cancer, the latter resulting from DNA mutations in skin cells caused by ultraviolet radiation. But melanin may have had a more direct impact on our ancestors’ ability to reproduce. Nina Jablonski and her husband, geographer George Chaplin, published a theory in 2000 suggesting that natural selection favored people with more melanin in places where ultraviolet radiation is more intense because ultraviolet radiation destroys an important nutrient—folate.20 We get folate, a type of B vitamin, from our diet, especially green leafy vegetables. Folate is required to make new DNA, which happens every time cells divide. That makes it especially important for pregnant women, because a growing fetus requires making a lot of new DNA. Folate deficiency is linked to birth deformities such as spina bifida and other defects of the neural tube, a structure that develops into various components of the central nervous

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system. Jablonski and Chaplin argued that having more eumelanin in the skin would minimize the destruction of folate in regions with intense ultraviolet radiation, such as tropical Africa. In such intense

So the earliest members of our species evolved dark skin. But

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the people who left Africa, as well as those who traveled to the south-

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and healthier ones, too.

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sunlight, people with more eumelanin would have had more babies,

ern end of the African continent, entered more temperate latitudes where sunlight hits the Earth more obliquely. The melanin in their skin became not only less necessary but a liability. That’s because ultraviolet light from the sun isn’t all bad. We need it, in fact, to produce vitamin D. Without enough vitamin D, we—like all vertebrate animals—are unable to absorb calcium and phosphate from our diets. These are nutrients used by the body in many different ways, including formation of the hard bones of our skeletons. People without enough vitamin D suffer severe health consequences, including the condition known as nutritional rickets, in which children’s bones fail to harden completely and become misshapen. In the skin cells of the epidermis and dermis, the absorption of ultraviolet light, specifically the wavelength known as UVB, triggers a biochemical reaction that results in the production of vitamin D by the liver and kidneys.

Having dark skin in a part of the world with less intense sun-

light makes it hard to get enough vitamin D, so natural selection favored a decrease in melanin production in people settling in the northern parts of Europe and Asia. As some groups made their way back into the tropics in parts of Southern Asia, Australia, Oceania, and the Americas, they once again found a need for better sun protection and evolved dark skin again. Jablonski and Chaplin’s major insight was to see melanin as a compromise—we need some protection from ultraviolet radiation to prevent folate damage but not too much so that enough radiation can enter the skin and trigger the production of vitamin D. According to this view, the beautiful diver-

sity of skin colors our species now possesses arose as a consequence of this basic evolutionary trade-off as our ancestors adapted to new environments.

Support for Jablonski and Chaplin’s tradeoff hypothesis came

first from the close correspondence between the intensity of ultraviolet radiation at the surface of the Earth as measured by satellites and measurements of the skin color of people from around the world. Not only could latitude accurately predict skin color, so did altitude—people living in mountainous areas experience more intense ultra­violet radiation and tend to have darker skin than lowlanders. Among the few exceptions to this general rule are the ­Eskimo-Aleut people of the North American Arctic, where sunlight is at its least intense—and yet they have relatively dark skin. Traditionally, the Eskimo-Aleut people have subsisted largely on a diet of marine mammals, fish, and caribou, all of which are rich in vitamin D, which likely explains why they did not evolve lighter skin. Vitamin D deficiencies leading to rickets and other health problems have become common among these populations as Western diets low in vitamin D replace traditional foods.

Genomic data also support the hypothesis that selection af-

fected pigmentation in human populations as they settled in different parts of the world. A gene called SLC24A5 that affects pigmentation in zebra fish was found to function similarly in humans. One particular single nucleotide polymorphism in the human version of this gene—having either a guanine or an adenine at a particular spot in the DNA sequence—varies substantially among populations. Between 98 percent and 100 percent of Europeans have an ade-

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nine at the site, whereas 93 percent to 100 percent of Africans, East Asians, and Native Americans have a guanine. Although other genes are now known to influence human skin color, SLC24A5 accounts for

lection, such as Sabeti’s long-range haplotype test, strongly suggest

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that this gene has experienced selection among Europeans.21

5 3

skin color between Europeans and sub-Saharan Africans. Tests for se-

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somewhere between one-quarter to one-third of the difference in



Intriguingly, the observation that East Asians and Europeans

tend to have light skin but different SLC24A5 genotypes suggests that different genetic mechanisms underlie skin pigmentation in these populations. The ancestors of modern Europeans and the ancestors of East Asians each independently evolved lighter skin, presumably in response to selection favoring a decrease in melanin production to enhance the production of vitamin D in these temperate regions. Here we have a case in which evolution caused a similar outcome in both populations but through a different genetic mechanism, a phenomenon that biologists refer to as convergent evolution.22 That it happened more than once strengthens the case that pigmentation evolved as a consequence of selection and not as a result of random drift, demographics, or surfing.

Modern development and industrialization have likely reduced

—but not eliminated—the importance of melanin for the survival and reproduction of people today, especially those living urban lifestyles. Clothing and shelter limit the amount of ultraviolet radiation people now experience. The widespread recognition that sun exposure can lead to skin cancer has prompted more extensive use of sunscreen, especially among lighter-skinned people living in or visiting regions with relatively intense ultraviolet radiation from sunlight. Nevertheless, skin cancer has become the most common form of cancer worldwide.23 There are more skin cancers diagnosed each year than all other forms of cancer combined, suggesting sun overexposure is still widespread.



Likewise, despite advances in our understanding of nutrition

and the availability of supplements, vitamin deficiencies remain common. Vitamin D deficiencies, which had become rare in the middle of the twentieth century, have since returned to pandemic levels.24 The widespread use of sunscreen, good for preventing overexposure to sunlight, is partly to blame—sunscreen with an SPF of 15 reduces the production of vitamin D by 99 percent. There is little information on the global incidence of folate deficiencies, though inadequate levels of folate have been found in the diets of pregnant women worldwide, especially in less developed regions.

One of the reasons these problems remain common despite

medical and technological advances that could prevent them is that many people today live in different regions than did their ancestors, and their skin is not well suited to the new environment. We move around the world more today than ever before in history. As of 2012, there were about 37 million flights each year, carrying nearly 3 billion passengers, 1.2 billion of whom crossed international borders. Most of these passengers are traveling for business or pleasure and return home, but an increasing number do not. As of 2013, there were approximately 232 million people living in a country other than the one in which they were born. The number of international migrants has continually grown, increasing by between 1.2 percent and 2.3 percent per year since 1990. Wealthy nations like the United States and Germany are the recipients of the majority of these migrants, where large urban centers such as my hometown of Houston have become something of a microcosm of global diversity.25

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Not only has all this globetrotting led to mismatches between

the melanin content of people’s skin and the amount of ultraviolet radiation they experience, it also means that human populations

tween people from different backgrounds are waning. Although race

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and ethnicity are poor proxies for human populations, the statistics

5 5

At the same time, in many places stigmas about relationships be-

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have opportunities for mixing that are unprecedented in our history.

on interracial marriages nevertheless provide an indication of how gene pools from once-distinct populations are melding together. In 2010, 15 percent of new marriages in the United States were classified as interracial, twice the percentage of 1980. Between 2008 and 2010, nearly one-third of interracial newlyweds included at least one partner who was an international immigrant. Predictably, these trends have been accompanied by an increase in the number of multi­racial babies, up from 1 percent of all births in 1970 to 10 percent in 2013.26

The mixing of genes from different populations is yet another

mechanism of evolutionary change, which biologists refer to as gene flow. The flow of genes between populations reduces the differences between them and brings new variation for selection to act on. Given how interconnected populations have become, it is clear that gene flow plays an important role in our continuing evolution.

Although it is now easier to move around the world than it

was before the invention of trains, planes, and automobiles, population movements have long been a big part of human history. In the last fifty thousand years, our species spread to nearly every habitable piece of land as well as to some places that hardly seem habitable. Indeed, our species has found ways to live in even the harshest environments, including high in the mountains where the thin air means that less oxygen is available to breathe.27

The decrease in oxygen is why people traveling from low to

high altitude often feel sick and, in some cases, can suffer more severe health consequences. I once experienced this situation myself when

I traveled to Peru as a graduate student on a research expedition. Our destination was the Amazon rainforest, but our ­jumping-off point was the city of Cusco, the ancient capital of the Inca Empire, which sits in a valley some 11,155 feet in the Peruvian Andes on the western edge of the Amazon Basin. I didn’t expect to have any problems with the altitude since I had been to Cusco once before and had felt just fine. This time, however, was different.

We flew in from the coastal city of Lima. As the plane landed in

Cusco, it rolled to a stop in front of the terminal, and then the crew opened the cabin doors. Immediately, I felt a wave of nausea pass over me as I began to breathe the thin air, which contained about a third less oxygen than at sea level. The nausea lasted the rest of the day, and I felt embarrassed and useless because I had to lie still in the front seat of the truck as my colleagues went around buying supplies to prepare for our expedition. It wasn’t until we began to descend in altitude a couple of days later, driving down the eastern slope of the Andes into the Amazon Basin, that the increase in oxygen helped me to feel normal again.

I was suffering from acute mountain sickness, a common occur-

rence among travelers who visit high altitudes without allowing sufficient time for the body to adjust. It takes the body several days to begin to compensate for the drop in oxygen, and several weeks or more to become better acclimated. Part of the adjustment involves making more red blood cells, since the hemoglobin they carry contains iron that binds to oxygen from the atmosphere and transports it around the body to the places it is needed. The more hemoglobin you have in your blood,

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the better you are at harvesting the oxygen that enters your lungs.

Why was I experiencing acute mountain sickness on this trip

when I had been fine the last time? My previous trip had been with

few more touring the slightly higher-altitude city of Arequipa be-

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fore taking an overnight train higher up into the Andes. I remem-

5 7

our time getting to Cusco, spending a few days in Lima and then a

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some friends shortly after graduating from college. We had taken

ber feeling my pulse and my breathing quicken as the train climbed into progressively thinner air, my body doing what it could to get more oxygen to my struggling cells. But by the time we made it to Cusco, I felt fine—my body had already had more than a week to increase the amount of hemoglobin in my blood, so the thin air did not bother me.

After several weeks, most people become fairly well acclimated

to the thin air at high altitude. It is for exactly this reason that some elite athletes train at higher altitudes before big competitions—they get a boost in their red blood cell concentrations that last for at least a few weeks, potentially giving them an edge when competing at lower altitudes.28 Being born and raised at high altitude is even better, because the body develops in ways that help compensate for the thin air—for example, by growing larger lungs that can harness more oxygen per breath. This is true for anyone, regardless of where their parents came from, although we now know that people whose ancestors have lived at high altitudes for hundreds of generations have had a chance to adapt to the low-oxygen environment not only by acclimatization but also through natural selection. Amazingly, this has happened not just once but at least three different times in separate parts of the world—and is likely still happening today. ■ The study of human adaptations to high-altitude environments made a great leap forward in 1962, when anthropologist Paul Baker

moved to Peru from State College, Pennsylvania, with his wife and four children.29 He was on a Fulbright fellowship and also had funding from the U.S. military which, since the outbreak of conflicts in the mountainous border regions between India, Pakistan, and China, had developed a sudden interest in how the human body responds to high altitudes. After a few months of living and working in other parts of the country, Baker and his family moved to Cusco, where he began collecting data on people living in the surrounding region. For the next ten years, Baker and his graduate students collected an extensive amount of information on the biology, health, and fitness of the local population—as well as of themselves—in an effort to understand the effects of high altitude on the human body.

Baker was not the first to investigate the biology of people

living at high altitudes. Earlier in the century, Peruvian researchers, including Carlos Monge and Alberto Hurtado, had studied the physiology of high-altitude Peruvians. They documented a combination of physical traits—including a large chest and lungs and high concentrations of hemoglobin in the blood—that seemed to help Andeans function in the mountains. So much so, in fact, that Andean natives living at thirteen thousand feet actually have more oxygen in their blood than do native lowlanders at sea level. But they also found that longtime residents of high altitudes often suffer from a condition now known as chronic mountain sickness that stems at least in part from having too many red blood cells in circulation. In other words, making more red blood cells helps the body adjust to low oxygen, but having too many can lead to problems.

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Paul Baker and his students saw the traits present in native

Andean people as the result of both acclimatization and natural selection having played out over generations. Although they could not

the result of having lived in the mountains their entire lives. Some

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support for this idea came from comparing people who migrated

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documented in native highlanders were hereditary and not simply

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yet pinpoint the genetic basis, they suspected that the traits they

from high to low altitude or vice versa with people who moved between similar altitude regions and with those who never moved. Although the hemoglobin concentrations of highlanders dropped to lowlander levels when they moved down from the mountains, those who were born in the mountains retained their large chest volumes even when they moved downhill. The children of migrants were of particular interest—kids whose parents migrated from low to high altitude did not develop the same large chests as kids whose families came from the highlands.

One of Baker’s students, Cynthia Beall, wondered whether

people living in other high-altitude regions of the world adjusted to thin air in the same ways as Andean natives. It was the early 1970s, and Nepal and Tibet were beginning to open to foreigners, making it possible for the first time to compare the physiology of people from the two largest high-altitude regions of the world. Beall would have to trek for days to remote villages to collect blood samples and take measurements from isolated populations whose ancestors had occupied the region for millennia. The results were amazing—Tibetans were well adjusted to life in thin air, but their bodies had an altogether different way of dealing with the low oxygen than Andeans.30 The blood of Tibetans living at high altitude had less hemoglobin and carried less oxygen than the blood of Andeans. In fact, most Tibetans had less oxygen coursing through their veins than people at sea level, yet they functioned perfectly well while breathing air containing 40 percent less oxygen. How was this possible?



Beall began to test as many hypotheses as she could think

of to explain how Tibetans were able to thrive at high altitude despite having less oxygen in their blood. She found that Tibetans breathe faster than Andeans, in much the same way that lowlanders do when they first arrive in the mountains. But unlike lowlanders, whose breathing slows as they adjust to the thin air, Tibetans keep breathing heavily. Although breathing faster would seem to be a way of compensating for the decreased oxygen in the air by getting more air into the lungs in a given amount of time, the blood data showed that this was not the case.

Eventually, Beall found an answer. She discovered that when

Tibetans exhale, they have elevated levels of a gas called nitric oxide compared with Andeans and lowlanders. Nitric oxide causes blood vessels to dilate (it is what causes an erection), allowing more blood to flow through them and at a faster rate. Beall also found that the muscles of Tibetans had more capillaries, the thin network of blood vessels that are responsible for delivering oxygen to their cellular destinations. Together, these two factors—higher blood flow and more delivery sites—mean that Tibetans can function at high altitude as well as Andeans despite having less oxygen in each drop of blood. In fact, Tibetans seem to have an advantage over their South American counterparts in that Tibetans rarely develop the chronic mountain sickness that plagues Andeans. This makes sense, given that the condition is associated with elevated hemoglobin levels, which Tibetans lack.

Tibetans and Andeans thus came up with completely differ-

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ent solutions to the same problem of the thin air at high altitudes. Given that both populations have been living in these environments for a long time—according to archeological evidence, at least thirty

her colleagues hypothesized that natural selection had tweaked the

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physiology in both cases, but that each population had responded

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about eleven thousand years in the case of the Andeans—Beall and

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thousand years and possibly more in the case of the Tibetans and

differently.31 But they didn’t yet have the genetic data to prove that selection had acted.

Just as the genomic era was beginning, Beall and her col-

leagues began studying a third high-altitude population, the Amhara people of the Ethiopian Highlands, and found yet another pattern of physiological adaptation to cope with low oxygen.32 Like Tibetans, the Amhara had low hemoglobin levels, but the Amhara were distinct in that their blood had high levels of oxygen. Beall’s team also compared the Amhara, who have lived in Ethiopia’s Simien Mountains for more than seventy thousand years, to another ethnic group, the Oromo, who also live in the Simien Mountains but for only the last five hundred years. As expected, the Oromo did not have the same physiology as the Amhara, who have had more time for natural selection to operate. Rather, the blood from Oromo people resembled that of lowlanders who had acclimated to high altitude. Here was evidence for a third independent evolutionary origin of adaptation to high altitude. All signs pointed to natural selection having operated in different ways in each of these three high-altitude regions of the world. The only missing pieces of evidence were genomic data identifying the genes responsible for these traits and confirming that selection had acted on them.

Speaking at the Leicester conference in 2014, Beall’s collabora-

tor Anna Di Rienzo, an Italian geneticist at the University of Chicago, brought the crowd up to speed on what the genome data had to say regarding high-altitude adaptation. In 2010, three different research

groups working on the genetic basis of high-altitude adaptation in Tibetans each published their results within weeks of one another.33 The conclusions were largely the same—native Tibetans do indeed have genes that appear to be under selection. Different versions of these genes are found in Tibetans and closely related Han Chinese. Two genes in particular, known as EPAS1 and EGLN1, both of which are involved in sensing and reacting to the amount of oxygen that enters the body, stood out from the rest. Particular alleles were found to correlate with low hemoglobin levels typical of Tibetans and also showed the strongest signals of selection having operated in the recent past. The results of genome studies on Andean and Ethiopian people were less straightforward, but seemed to suggest that selection has operated in those populations as well but that their genetic response to selection, like the physiological profiles Beall and her colleagues had described, was different from the Tibetan pattern.

There is no easy way to compensate for thin air. Unlike variation

in ultraviolet radiation, which can be accommodated by using sunscreen and taking vitamin supplements, low oxygen is an unavoidable fact of life at high altitudes. Supplemental oxygen can be used for short periods of time, such as by mountaineers attempting to reach a summit or in the case of medical emergencies, but is not practical for continuous use. So for the more than 25 million ­people currently living above ten thousand feet, the same evolutionary pressures that led to adaptations in the past are likely still operating today.

Like skin pigmentation and infectious diseases, natural selec-

tion for traits that improve performance in low oxygen might be

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strongest during pregnancy, childbirth, and early childhood. Women from lower altitudes who give birth at higher altitudes are at greater risk of complications like preeclampsia, in which the mother experi-

give birth to heavier babies on average than do women from different

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ethnic groups who are living at comparable altitudes. Given that heav-

6 3

if untreated. Interestingly, Andean, Tibetan, and Amhara women all

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ences high blood pressure that can be fatal for both mother and child

ier babies tend to have better chances of survival, this suggests that selection has acted to improve birth outcomes in all three populations.

Indeed, even before they knew which gene was responsible,

Beall and her colleagues had found that living Tibetan women inferred to have an allele that affected how much oxygen was bound to the hemoglobin in their blood had more surviving children than those without the allele.34 This suggested that natural selection had not only caused highlanders to become adapted to their high-­ altitude environment in the past but that the selective process is still operating.

To understand where the genes that help Tibetans live at high

altitude came from, Beall collected samples from a neighboring population of highlanders, the Sherpa people of Nepal. The Sherpa are well known for their prowess in high-altitude mountaineering expeditions, having become the definitive guides and porters for foreigners attempting to climb Mount Everest and other Himalayan peaks. Di Rienzo and her team at the University of Chicago compared the Sherpa blood samples collected by Beall with samples previously collected in Tibet as well as with reference genome data from other populations collected as part of the HapMap Project.35 Their results suggested the Tibetans and Sherpa have some of the same genetic adaptations for high altitude, and that modern Tibetans seem to have originated from people who migrated up from the lowlands and then mated with highlanders, thus acquiring their beneficial high-altitude genes.



This was a major breakthrough. Di Rienzo and her colleagues

had found that beneficial genes could be acquired through sex rather than simply by mutation. Mutations happen—we do not yet know exactly how frequently they occur in humans, but a study comparing the genomes of children to both of their parents suggested that, on average, every baby is born with about sixty new mutations to their genes.36 Mostly, these changes are harmful or neutral, but on rare occasions they turn out to be helpful. What’s more, even beneficial mutations start out in just one individual and take a long time—many generations—to become common in the population. That baby would have to grow up to have children who also had the beneficial mutation, who would pass it on to their children, and so on. There is a good chance that the mutation will disappear from the population before it has a chance to become common. But there is also a chance that a helpful mutation might have already popped up somewhere else.

Mutations might be rare, but sex is not, and any time people

from different populations have children together, their children’s genomes become a mixture of genes from each population. The Tibetan data suggested that genes flowing from one population into another through sex can effectively jump-start the evolutionary process. To better understand our evolutionary future, then, we need to understand how genes flow between populations. ■ No one understands gene flow quite like David Reich. I visited his lab

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at Harvard Medical School hoping to get some perspective on how genes flowing between populations have affected human history and what it might mean for our evolutionary future. He met me at

cidedly modern next to the stately white marble buildings that con-

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stitute much of the Harvard Medical School campus. We climbed a

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New Research Building, a steel and glass structure that looked de-

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the security desk on the first floor of the rather uncreatively named

flight of stairs to the second floor, passed a large world map on the wall, and entered the lab. I noticed a pale blue light shining through a small window in a very solid-looking door to my left. This, Reich explained, is his ancient DNA lab. The blue light is from ultraviolet radiation, meant to destroy any DNA that might have been shed by a passing researcher and that could contaminate the precious samples contained within.

We made our way through the lab, where workspaces sepa-

rated by glass walls were covered with notes and equations scribbled in various shades of dry erase marker. Reich’s office was in the back, an elongated rectangle of glass overlooking Avenue Louis Pasteur. Reich explained how, thanks to advances in sequencing genomes from very old skeletons as well as improvements in the statistical methods used to evaluate them, his group has been working on the genetics of ancient human populations. By comparing DNA from hunter-gatherer populations that predate the arrival of agriculture in Europe to DNA from an early farmer from Germany, Reich and his colleagues demonstrated that modern Europeans resulted from the mixture of genes from at least three distinct populations.37

Our conversation was interrupted by a knock on the door. In

walked Nick Patterson, apologizing for the intrusion. Patterson is something of a legend in the genomics world, a big data guru with an unusual background. Originally from London, as a child he had an affinity for mathematics and chess. He attended Cambridge, completing a bachelor’s degree and then a doctorate in mathemat-

ics. He then worked for twenty years as a code-breaker, applying his mathematical expertise to top-secret communications projects for the British government and later for a U.S. government contractor before switching fields entirely—not just once, but twice. Using his ability to analyze patterns in complex data, Patterson went to work for a New York hedge fund where he helped to predict stock market fluctuations in the 1990s. In 2000, Patterson decided to apply his code-breaking skills to yet another type of complex data—human genomes.

Patterson and Reich became close friends and colleagues, and

the pair was recruited by Svante Pääbo, an expert in ancient DNA, of the Max Planck Institute in Germany to work on the Neanderthal genome, which Pääbo’s lab had sequenced using fragments of DNA retrieved from fossil bones. Reich and Patterson used the genome data collected by Pääbo’s lab to show that the genomes of modern humans outside of Africa contain between 1 and 3 percent Neanderthal genes, a stunning discovery that implied that humans and Neanderthals mated and had surviving offspring. DNA recovered from a modern human skeleton in Romania suggested that gene flow between modern humans and Neanderthals may have continued until as recently as forty thousand years ago.38

This discovery was only a beginning. In 2010, the team an-

nounced it had documented another case of gene flow between modern humans and a different extinct type of hominin, called Denisovans, discovered in a cave in Siberia. According to the genome data, Denisovans were related to but distinct from Neanderthals,

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and Denisovan genes could still be found comprising as much as 5 percent of the genomes of modern people living in Oceania and nearby regions. Subsequent work would suggest that genes have

thals and Denisovans.39

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and between Denisovans and humans, but also between Neander-

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flowed back and forth not only between Neanderthals and humans

Gene flow, Reich explained to me, has been the rule in human

history, not the exception. Now that it is possible to examine the genomes of ancient people and make comparisons with modern populations from around the world, the emerging conclusion is that our gene pool has always been something of a melting pot. Periodically throughout history, people from different regions somehow came together and had children, and so seemingly isolated human populations never really remained isolated for very long. We now know that our ancestors swapped genes with other humanlike species they encountered in their travels. Our species, you might say, has been rather promiscuous.

What’s more, some of those ancient interspecies trysts may

have allowed our ancestors to acquire helpful genes. The clearest case so far comes from work by Danish population geneticist Rasmus Nielsen, one of the researchers who worked with Pääbo, Patterson, and Reich on gene flow between Neanderthals and humans, in collaboration with researchers at a massive genome-sequencing center in China.40 In 2010, their team was among the first to discover the version of EPAS1 responsible for high-altitude adaptation in Tibetans. Nielsen was surprised by how different the Tibetan version of the gene was—it contained five distinct mutations not found in any other known human population. When the Denisovan genome was published, Nielsen and his colleagues were even more surprised when they discovered that it contained all five mutations in the EPAS1 gene found in Tibetans. This uncanny similarity was unlikely to have happened by chance, and the long stretch of similar DNA

sequences suggested that the two populations—Denisovans and modern Tibetans—must have exchanged DNA fairly recently. Here was strong evidence that the beneficial genes found in modern ­Tibetans—the genes that Anna Di Rienzo’s team knew had come from another population—actually came from another species. ■ The new environments our ancestors encountered as they spread around the world—the thin air at high altitudes, different amounts of ultraviolet light, and all manner of infectious microbes—created challenges for their survival. Solutions to these challenges came by way of various combinations of mutations, gene flow, and natural selection as well as aspects of culture. Thanks to our ingenuity, we developed agriculture, domesticated animals, established civilizations, invented machines, and discovered medications. We passed on our acquired knowledge, each generation learning from its predecessors and building upon it. Culture, like genes, is heritable and has joined natural selection as a dominant force creating change in our species. In thinking about how evolutionary processes continue to affect people today, and how they will operate in the future, it is tempting to believe that the influence of culture means that what happened in the past is no longer relevant.

But culture can also be an agent of evolutionary change.41

What we eat, for instance, is an important element of culture. Dairy products are a dietary staple in northern Europe but until the last century or so were rare in other regions, such as East Asia. The ability

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to digest milk as an adult varies considerably around the world, and it is no coincidence that dairy consumption is higher in places where the ability to digest raw milk is more common.42 Lactose intolerance

human babies, being the mammals that we are, produce lactase,

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the enzyme required for lactose digestion. But in most mammals,

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able to break down lactose, the sugar contained in raw milk. All

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prevents about two-thirds of the world’s population from being

lactase stops being produced around the time that mothers wean their babies. People who can drink milk as adults simply never stop making lactase, thanks to a small evolutionary change in the genomes of their ancestors.

Diets changed for many people around ten thousand years

ago when some populations began to grow crops and raise livestock. Although agriculture meant food sources became more abundant and reliable, early farmers were not necessarily well equipped biologically for digesting what they harvested, including milk from cattle, sheep, and goats. Consuming animal milk would have given dairy farmers a sustainable source of energy, clean water, and nutrients such as calcium. Although lactose content is reduced in the making of products like yogurt and cheese, making these easier for anyone to digest, people who could consume any dairy without having digestive issues like diarrhea would have had a survival advantage. So, selection favored the ability to drink milk as an adult and, generation by generation, adult production of lactase became more common in pastoral cultures.

Beginning in the 1970s, researchers began to find evidence

that a single gene controls lactase production. The molecular genetics of the gene, known as LCT, were worked out in the 1990s and early 2000s, and it would soon become one of the first genes identified as having experienced selection using the new techniques developed by Pardis Sabeti and others. A study using DNA from modern people as well as DNA extracted from ancient Eurasian skeletons found that

the strongest signal for natural selection came from the LCT gene— and that the earliest appearance of the version of the gene that allows adults to digest milk was between 2450 and 2140 BC, suggesting that selection has been acting on this gene within the last four thousand years. Interestingly, the version of the LCT gene common in Europe was not found in non-European populations where adults consumed milk products, such as some Africans. A group led by human evolutionary geneticist Sarah Tishkoff found that a different mutation in the LCT gene gave east African pastoralists the ability to digest lactose just as well as Europeans, and that it, too, had become more common because of natural selection.43

The rise of agriculture made grains a more significant portion

of diets in some cultures, such as along the Yangtze River in China where rice was first domesticated. Like most grains, rice contains a lot of starch, which must be digested using particular enzymes. One of these, salivary amylase, is produced by a gene that comes in different numbers of copies—ranging from two to fifteen—in different populations. In populations like the Han Chinese and the Japanese, in which starch has historically been a significant portion of the diet, people tend to have more copies of the amylase gene and consequently make more of the digestive enzyme. This correlation suggests that natural selection may have played a role in the differences in amylase production between modern human populations.44

So rather than buffering us from experiencing natural selec-

tion, our intelligence and ingenuity have actually prompted evolutionary changes in our biology. And if dietary adjustments have

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played a major role in natural selection on our species in the past, we should consider the role of diet in our ongoing evolution. We are currently in the midst of a global dietary shift that may rival the de-

beverages, which began in more developed countries like the United

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States and are spreading rapidly into less developed regions, is

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The widespread consumption of processed foods and high-calorie

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velopment of agriculture in terms of its impact on human health.

closely linked to a growing pandemic of obesity, diabetes, and cardiovascular disease. Given that these conditions have replaced infectious diseases as the leading causes of death in developed nations, natural selection may continue to play a role in tweaking our biology through our diet.45 ■ Leaving the conference at Leicester, I had a new appreciation for the insights that the big data era of genomics has provided into our evolutionary past. We now know that natural selection helped our ancestors become better adapted to new environments as our species spread from its birthplace in Africa. There are some cases— like the thin air at high altitude—in which the force of natural selection operating in the past is likely to be just as strong today, and others—like ultraviolet radiation and diet—in which modern life has likely modified its impact. But we also know that other evolutionary forces—namely, genetic drift and gene flow—played important roles in the creation of our common gene pool.

The message from the world of human evolutionary genomics

seems to be that our species has a long history of moving around the world, adapting to local conditions, and swapping genes with neighbors. In some sense, then, our species today is doing what is has always done. But there are also important differences between our history and what is happening today. The number of individual people alive at any one time has grown exponentially, and our current

massive population size means that, with the birth of each new baby, there are more new mutations entering the gene pool today than ever before. As we have seen, we also move around the world at rates that are unprecedented in human history, bringing our genes, cultures, and diseases with us. Taken together, these trends suggest that our species is entering an era in which there is more genetic variation—the raw material for evolutionary change—than ever before.

But we are also entering an era in which many of the rules

of the past no longer apply. Given all the changes we have experienced, even in just the last several hundred years, extrapolating from the past does not tell us everything about how our species is evolving today. To understand how human evolution proceeded into the modern era, we would need a different type of information—and it

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would come from a most surprising source.

3 . World in Transition

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enomic information suggests that human evolution has continued into recent times, but extrapolating from the past cannot tell us whether it is still occurring. One place that could is the archives of the Roman Catholic Church’s Canadian headquarters in Quebec City. Which is why evolutionary geneticist Emmanuel Milot took me there to explain how he dis-

covered that people living on an island in the Saint Lawrence River have been experiencing natural selection since the start of the nineteenth century.

I arrived in Montreal late on a Wednesday afternoon. Milot

met me at the airport and took me to dinner at a microbrewery downtown. There he told me his story. As a graduate student, he had worked on the genetics of a seabird called the wandering albatross that lives in the Kerguelen Islands, a rugged archipelago in the southern Indian Ocean near Antarctica. He spent months at a time on French research vessels traveling to distant parts of the archipelago taking blood samples and other measurements of the birds. He explained that he once caught an albatross with a band around its leg indicating it had been alive and breeding before Milot was even born. Working with such a long-lived species made him wonder about issues that are particularly crucial to animals with longer lives, such as how long it takes for a young bird to be able to repro75

duce and how the body begins to break down with old age. These thoughts prompted him to wonder about other long-lived species, like humans.

After Milot completed his dissertation research on the wan-

dering albatross, his interest in the evolution of so-called life-­history characteristics, such as the timing of reproduction and death, prompted him to switch to studying humans. But collecting such data on people is quite different than working with birds, so Milot teamed up with anthropologist Francine Mayer, whom we visited the next morning. Over a breakfast of croissants and coffee in the flower-filled garden behind her house, Mayer explained how, in the 1960s, she was part of a research group that started to search for isolated communities where records were available on a fairly small population over multiple generations. They found just such a community on an island known as Île aux Coudres. Although it is only a mile and a half from the north shore of the Saint Lawrence River, dangerous currents and icy conditions during part of the year kept its inhabitants from being as closely connected to nearby villages as were other communities. What’s more, another researcher, Pierre Philippe, had visited the island in 1967 and obtained permission from the community and from the local priest to transcribe parish birth, death, and marriage records for demographic research.

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Together with a graduate student named Mireille Boisvert, Mayer worked for three years in the early 1990s to construct a validated genealogy of the inhabitants of Île aux Coudres that included more than eight thousand births and two thousand marriages from the 1720s through the 1960s.

Milot joined the research team as a postdoc in 2009 and, using

a subset of the population records, discovered a surprising trend in

1800 and 1939, the average age at which women became mothwomen on Île aux Coudres who started having children at younger ages also had larger families. Intriguingly, their daughters tended to do the same. Milot knew from his studies of birds that the timing of reproduction is a trait that often responds to natural selecleft by an individual. To prove that natural selection had caused the change, he would need to show that there was a genetic basis for the decrease in age at first reproduction and that factors other than natural selection, including genetic drift, changing cultural practices, or improving nutrition and health care, did not fully explain the changes. Using a mathematical model borrowed from the study of animal breeding, he was able to tease apart these factors.1

The model predicted how similar any two individuals should

be based on how closely related they were, taking into account their similar environment. This allowed Milot to calculate the predicted breeding value of age at first reproduction, which is an estimate of the extent to which the value of that trait is explained by a person’s genes, and how it compares to the population average. If, for example, a particular woman had her first child at age twenty-three, and the average age at first reproduction in the population were twenty-five, her breeding value would estimate how much of that two-year difference was inherited from her parents. Over eight generations, the average predicted breeding value dropped significantly, suggesting an evolutionary response.

Using infant and juvenile survival rates as a proxy for overall

health, Milot and his colleagues found no evidence that the popu-

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tion because it has such a strong impact on the number of offspring

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ers dropped from twenty-six to twenty-two. It seemed that those

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the birth data. Over just a few generations of people born between

lation’s health was changing in a meaningful way over this period. Cultural differences could be ruled out because the small, tight-knit community on the island shared the same heritage, language, religion, diet, and other practices. The team also excluded the possibility that genetic drift could account for changes in age at first reproduction by determining from their models that it could not have had as large an impact on the age of first reproduction as the change they observed. The best remaining explanation for the observed decrease in the age at first reproduction was evolution by natural selection.

I wanted to see the evidence for myself, so Milot and I drove

through the cobblestone streets of the historic lower Quebec City and up a steep hill to the massive complex of five-story stone buildings that constitute the Archdiocese of Quebec, the central administrative branch of the Roman Catholic Church in Canada. There we met diocesan archivist Pierre Lafontaine, who was casually dressed and spoke quietly, apologizing for his English, which he rarely has occasion to use. Lafontaine led us into a large room with three tables forming a crescent, where he had set out several books in anticipation of our visit.

On one table sat a scruffy-looking book with a handwritten

label on the cover that read, De 1859–1866. A second, typed label indicated that the book contained records of the baptisms, weddings,

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and funerals from those years—the raw data Milot and Mayer had used. Lafontaine then led us into a long, narrow room containing row after row of cataloged volumes—like the stacks of a modern ­library—of parish records like the book we had just examined. Here was an incredible source of information about the people of Quebec that spanned more than a dozen generations. It was the sort of data that evolutionary biologists dream of—information Milot

­humans.

The idea to use multigenerational church records to study human demography was first suggested by an Italian priest in 1951 while attending a lecture by geneticist Luigi Luca Cavalli-Sforza. Over the to examine how marriages between relatives affected the distribution of particular genes throughout Italy. Beginning in the 1990s, researchers in Finland such as Virpi Lummaa began extending this approach, using local parish records to look for evidence of natural selection having operated in preindustrial Finnish communities from the eighteenth and nineteenth centuries.2 They did indeed find data that suggested opportunities had existed for natural selection to act on the timing of reproduction among women in these communities, including evidence that natural selection may have acted differently on the wealthy versus the poor, but they could not be certain that selection had actually had any effect.

Detecting a response to natural selection was complicated,

partly because of the need for sophisticated statistical analyses that can differentiate between the various factors that can cause traits to change through time. In the 2000s, researchers studying wild animal populations began testing for a response to selection using multigenerational data, but the early methods turned out to be unreliable. Jarrod Hadfield, an evolutionary biologist at the University of Edinburgh, developed a statistical method, building on Bayesian generalized linear mixed models to estimate trends in breeding values, that solved the problem.3 Milot met Hadfield at a small confer-

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next several decades, Cavalli-Sforza and his colleagues used this idea

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could never hope to obtain for albatrosses or any species other than

ence in the Italian Alps in 2009, and Milot was eager to try the new method on the data he had just acquired from Francine Mayer on the population at Île aux Coudres. As soon as he got home to Montreal, he took his laptop to a café and tried it out. When he saw the result—the first evidence that a historical human population had responded to natural selection—he nearly spilled his espresso. ■ The next day Milot and I continued our journey toward Île aux Coudres. We drove aboard the Joseph-Savard, one of two car ferries in operation on the busy Saturday morning, named for one of the island’s original settlers. Savard and his wife were one of thirty families that first arrived on the island between 1720 and 1773. The island’s population grew rapidly over the next few decades, and families were forced to divide what little land there was among their children.4 Unlike settlements on the mainland, which could keep expanding as their populations grew, the Saint Lawrence was a rigid barrier and families were reluctant to set up farms on the other side. On the clear summer day of my visit, it was difficult to imagine how dangerous the river can be, but the low tide had exposed a few rocks, and the swirls and ripples around them hinted at the strong currents that make this section of the Saint Lawrence so treacherous. It is es-

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pecially dangerous in winter when the river fills with floating chunks of ice.

Twenty minutes later, we drove off the ferry and onto the is-

land’s main road. When we reached the southern end, we stopped at a small boulangerie whose pleasant-looking patio with wooden picnic tables beneath red umbrellas overlooked the river. As Milot and I entered the bakery, a smiling woman approached us and introduced

has always lived on the island, then pointed excitedly to a nearby the white fluffy seeds from a dandelion. The photo, she explained, was a screenshot from the first of a series of famous documentaries by Pierre Perrault about the island—and she was the girl.5 She had purchased the bakery nine years ago from the family that first name—Boulangerie Bouchard.

The bakery was certainly doing good business with the week-

end tourists, who had become a major source of income for islanders.6 Tourism to the region began back in the second half of the nineteenth century, as wealthy Americans looking to escape uncomfortable summers in the crowded cities of the northeastern United States began visiting the Charlevoix region that includes Île aux Coudres. This new source of income meant that islanders were no longer dependent on farming and fishing to make a living. By the 1960s, when the Perrault documentaries were filmed, many of the seafaring traditions of generations past had nearly been forgotten.

Leaving the bakery, Milot and I headed south toward the

village of Saint Louis where we passed a cemetery with tombstones that repeated just a handful of names—Harvey, Tremblay, Boudreault, Dufour, Pednault, Mailloux, Desgagnés—a reminder of how small this community had been. But while the village’s houses and stone church looked much the way they did in photos from the early 1900s, it was clear from our brief visit that the twenty-first century had arrived on Île aux Coudres. Our hotel had WiFi, and we navigated around the island using the GPS technology in our cell phones. A silver-haired man sitting in a rocking chair on his front porch near

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opened it in 1945 but, with an eye toward history, kept the original

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wall with a framed black-and-white photo of a young girl blowing

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herself as the owner. She explained in rapid French that her family

the church waved to us and offered a friendly bonjour just as I imagine his grandfather would have one hundred years ago—only his grandfather would not have first removed his iPod headphones.

Modernization meant that the conclusions made by Milot,

Mayer, and their colleagues about natural selection in humans could not be so easily extended to the people living since the second half of the twentieth century. In their research article, Milot and his colleagues emphasized that the island inhabitants experienced natural fertility, meaning that no effective forms of birth control or family planning were available. Medicine, technology, education, and other benefits of industrialized life meant that the age at which a woman had her first child became influenced by a great many factors, not just genetics. Around the world, as economic development proceeded, the average age at which women become mothers has increased—the exact opposite of the pattern found by Milot and his colleagues.7

At least part of the reason for the delay in starting families

among women in more developed regions is education—when women spend more time in school, they tend to start having children later in life. Other factors include better career opportunities and access to contraceptives. One of the consequences of delaying reproduction is that women who start having children later tend to

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have fewer children over the course of a lifetime. Indeed, one of the hallmarks of modern industrialized societies is smaller family size. As of 2013, North American women averaged 1.8 children and European women averaged 1.6, compared with 5.3 and 6.7 children in Latin America and Africa, respectively.8 As development improves access to clean water and modern health care, reducing the burden of infectious diseases, death rates decline as well. When falling birthrates

occurs.

Demographic transitions began affecting human populations around the world in the nineteenth century. Evolutionary biologist Jacob Moorad used birth and death records from a population database 1850. Moorad’s mathematical models found that during the transition the opportunity for natural selection grew stronger. Specifically, he discovered that the component of selection contributed by differences in survival decreased by 37 percent, while the component ­contributed by differences in fertility increased by 45 percent.9 In other words, in nineteenth-century Utah, the demographic transition meant natural selection became less about how long people lived and more about how many children they had.

Economic development continued to trigger demographic

transitions into the twentieth century. In 1974 the United Kingdom’s Medical Research Council established a clinic in a rural village in the West African nation of Gambia. The clinic provided free health care to local residents and was largely run by Ian McGregor, a doctor who had been working in Gambia since 1949. The clinic had a major impact in improving the lives of the people living nearby, especially for pregnant women and young children. The mortality rate for children under the age of five declined from more than 40 percent to less than 10 percent. Birthrates declined as well, indicating that a demographic transition was under way—triggered in part by the establishment of the clinic.

McGregor had collected all manner of information about the

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to show that such a transition took place in Utah beginning around

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follow soon after a decline in death rates, a demographic transition

local population in his effort to understand and control malaria and other diseases. The clinic workers also measured the height and weight of all patients who came in for their annual medical exams. The Gambia data included information about the same people over a period of fifty-five years, beginning before the demographic transition had begun and ending after its completion. Yale biologist Steve Stearns and colleagues used these data to demonstrate that before the demographic transition, natural selection favored women who were shorter and heavier but afterward the opposite was true—­ selection favored women who were taller and thinner.10 Just as in nineteenth-century Utah, the demographic changes altered the opportunities for natural selection—only in this case, it actually reversed its direction.

Stearns had become interested in contemporary human evo-

lution in the mid-2000s because he was frustrated with physicians who, he felt, were making the incorrect assumption that human evolution had ended and that our biology was essentially frozen in time. Stearns had worked on the evolution of life-history events like the timing of reproduction, first in Hawaiian mosquito fish and later in fruit flies, and his work suggested that evolution can operate much more rapidly than was previously thought. He thought the same principles might apply to humans and was looking for a modern

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human population where he could look for evidence of ongoing evolution. Given that most human populations have already undergone demographic transitions or are in the midst of one, documenting natural selection in a population that had already experienced a demographic transition would provide the best possible insight into our evolutionary future. In 2007, geneticist Diddahally (Raju) Govindaraju visited ­ opulation. Stearns’s office and told him about just such a p

Govindaraju was a geneticist involved in a study by the Na-

tional Heart, Lung, and Blood Institute that had collected nearly six of Framingham, Massachusetts. The study had begun in the middle of the twentieth century, when cardiovascular disease surpassed infectious diseases as the number one cause of death among Americans. The medical community wanted to find out not only what ease but also whether there are particular factors that make some people more susceptible to it than others. An initial group of 5,209 volunteers were recruited to participate in 1948; they agreed to return every two years for a medical exam and questionnaire. A second cohort was recruited in 1971 from the children of the first cohort. Both groups continue to return every two to four years to the two-story, L-shaped building for their checkups, making the Framingham Heart Study the longest-running multigenerational study in medical ­history.

It was exactly this reason that Stearns found the Framingham

data so enticing. Because the same people were examined multiple times throughout their lives, and because the data also included the children of the first cohort, Stearns and Govindaraju, along with postdoctoral researcher Sean Byars and demographer Doug Ewbank, were able to look for changes that were heritable and affected survival and reproduction. And they found them—compared to the population averages, parents and their children tended to be more similar to one another in many of the traits that had been measured in the study. What’s more, women differed in how many children they had during their lifetimes, with some women having no children and others having as many as nine. Those differences meant women who had more children had a greater influence on the traits

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was responsible for the increased prevalence of cardiovascular dis-

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decades of life history and health data from people living in the town

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in the next generation. The women who had the most children were those who were, compared to the population averages, somewhat shorter and heavier, with lower total cholesterol and systolic blood pressures, and who began reproducing earlier and experienced menopause later. In short, Stearns and his colleagues had found that natural selection has continued to operate in Framingham.11 Ironically, but much to Stearns’s delight, it was medical data that proved ­doctors could no longer assume that human evolution has ended.

Interestingly, the Framingham data revealed that even in a

population that had already experienced a demographic transition, the intensity of natural selection on some traits could change during the span of just a few decades. The strength of selection favoring lower total cholesterol levels, for instance, declined in the Framingham population between 1950 and 1990. Stearns and his colleagues suggested that this change may reflect shifts in diet and exercise that resulted from public health campaigns aimed to educate people about the close relationship between these practices and their cardiovascular health—a connection that had come from data collected in the Framingham Heart Study itself. Here was another example of how cultural practices can influence how natural selection operates.

Cultures can change fast—consider fashion—so Stearns and

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his colleagues noted that the influence of culture on natural selection makes it difficult to predict how natural selection will continue to operate long into the future. Nevertheless, their data allowed them to make projections about how the traits currently under selection are likely to change in the next few generations. If current trends continue, they predicted, in ten generations women in Framingham would be about 1.3 percent shorter and 1.4 percent heavier, and their

by 3.6 percent and 1.9 percent, respectively. They also predicted that younger when they have their first child and about ten months older when they go through menopause. These are rather modest changes; natural selection in Framingham, unlike in Stearns’s fruit flies and mosquito fish, seems to be acting quite slowly. Although the precise predictions about future changes in

particular traits were intriguing, the conclusion from Framingham was that natural selection continued to operate in an industrial New England suburb with the low birth and death rates that characterize a population that had already experienced a demographic transition. Just as in Utah and Gambia, after the demographic transition most children who were born survived to adulthood, so the relative strength of selection on traits that affect survival was low. Traits affecting fertility, on the other hand, were under stronger selection.

Of the traits under selection in Framingham, the two most ob-

viously linked to fertility are the age at first reproduction and the age of menopause. The fact that selection favored an earlier age at first reproduction for women in Framingham, just as on Île aux Coudres, suggested this trait might not be affected by the demographic transition. Indeed, Stearns, Byars, Govindaraju, and Ewbank wrote a review article in 2010 that summarized the fourteen studies to date that looked for evidence of natural selection in contemporary human populations, finding that age at first reproduction was among the traits most frequently identified as being under selection in both preindustrial and industrial populations.12 In addition to their Framingham data, five other studies had found evidence that natural selection favored an earlier age at first reproduction, and

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women in ten generations would, on average, be about five months

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total cholesterol levels and systolic blood pressure would decrease

three of the five—from the United States, Australia, and Europe— were in postindustrial populations from the twentieth century.

Interestingly, despite consistently finding that selection has fa-

vored an earlier start to reproduction, the actual age at which women are becoming mothers has mostly been rising. In the ­thirty-four nations that constitute the Organization for Economic Cooperation and Development, the average age at first birth went up from ­twenty-four to twenty-eight between 1970 and 2008. Differences in the age of new mothers are strongly correlated with education. In the United States, 62 percent of women who did not attend college had their first child before the age of twenty-five, while the median age for women with a bachelor’s degree was twenty-eight and among women with a master’s degree or higher, the median age was thirty.13

This discrepancy suggests that although there have been op-

portunities for selection to act, there has not yet been a response to selection in industrial populations in the same way that Milot and his colleagues found for preindustrial Île aux Coudres. The discrepancy also highlights the tension between cultural and evolutionary forces in modern society, which in this case are in direct opposition. As Stearns explained it during a conversation on Skype, “Biology is telling women that they will have more grandchildren if they mature earlier, while culture is telling women that they will have more

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successful careers if they mature later.” We do not yet know how the dynamic between these two opposing forces will play out. What we can say, however, is that the complex interactions between culture and natural selection will be increasingly important for the future of our species.

Combined with an earlier start to a woman’s reproductive

years, the predicted increase in the age at which women experience

in the future, women in Framingham are predicted to have a larger is particularly interesting, though, because it highlights a peculiarity about human reproductive biology. We are the only ape, and one of only a few mammals, in which females regularly live for many years after losing the ability to reproduce.14 Menopause is not only unuwhich acts to increase reproductive output, favor a trait that causes a reduction in the ability to produce offspring?

Evolutionary biologist George Williams suggested a solution

in 1957 based on the observation that childbirth can be dangerous, and that the risk to the mother increases with age.15 The risk to human mothers is greater than to mothers in other species because our big heads make human childbirth especially dangerous. Older women who had already had kids, Williams argued, might be better off from an evolutionary perspective if they stopped having more children of their own and instead focused their energy on raising their grandchildren. If a woman invests in her grandchildren’s survival, those grandchildren would be more likely to grow up and have kids of their own. A woman could therefore leave behind more great-­ grandchildren by helping to care for her children’s children than if she risked trying to have more kids of her own.

In contrast to this “mother hypothesis,” which focused on the

risk to mothers of continuing to reproduce, anthropologist Kristen Hawkes proposed an explanation for the menopause puzzle that centered on the importance of grandmothers. She explained how it happened over a meal of spicy Thai soup near her office in Salt Lake City. Hawkes was working with the Hadza, an indigenous group that

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sual but also an evolutionary puzzle—how could natural selection,

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window of opportunity for having kids. The later age of menopause

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menopause—ending the possibility of reproduction—means that

lives a traditional hunter-gatherer lifestyle in Tanzania. She was interested in how they acquired food, and in particular how much time was spent on different food-related tasks by the various group members. Her work revealed that women and girls spent a lot of time collecting food, particularly the older women, who spent much of the day digging tubers out of the rocky soil. She found that the amount of time a mother spent foraging had a direct impact on the health of her children, but mothers with young babies were less effective at providing food for their older children. Grandmothers, however, made up the difference by supplying their grandchildren with tubers and other food, allowing Mom to focus her energy on her baby until it was weaned.16

Hawkes’s study of the Hadza provided a direct mechanism

by which grandmothers might help to increase the number of descendants they leave behind. Because they did not have to wait for their children to become self-sufficient before having another baby, women whose mothers were helping provide food could have more children over the course of a lifetime. Although her observations were from a modern group of people and so could not directly show that help from grandmothers caused the evolution of menopause in our ancestors, a computational model she developed with mathematician Peter Kim suggested that this factor might have been sufficient

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to do so.17 Their model began with a hypothetical ancestral species with a lifespan like that of a chimpanzee, in which fertility gradually declines with age and ends around the time of death. By adding in the benefits provided by grandmothers, their model showed that the lifespan could evolve over many generations to one that resembles that of humans, in which the life expectancy extends far beyond the age at which reproduction ends.

A hypothesis proposed in 2012 to explain primate behavior

turned Hawkes’s hypothesis around. Whereas her grandmother ural selection to favor an extended postreproductive lifespan, the self-domestication hypothesis suggests that selection against antisocial behavior could favor an extended lifespan, which made it possible to be a dedicated grandmother. Yet another hypothesis to Stearns and doctoral student Dieter Ebert based on the observation that the genetic quality of eggs declines as a woman ages because the mechanisms used for quality control begin to break down. This process could cause natural selection to favor quality over quantity, as it were, if children born to older mothers suffer genetic defects that impair their chances of survival or rate of reproduction.18

Although each hypothesis suggests a different reason for nat-

ural selection originally favoring menopause, the data from Framingham suggest that the evolutionary benefits of menopause that must have existed in the past no longer outweigh the costs. The dangers of childbirth have been greatly diminished for women with access to modern health care. Hawkes pointed out that in many modern societies, grandmothers are playing much less of a role in raising their grandchildren than they do in traditional societies, which are thought to have family structures similar to those of our ancestors. There are many factors at play, but in part this seems to be due to changing residential patterns affecting how close grandparents live to their grandchildren. In the United States, 57 percent of people aged sixty-five and older lived in a multigenerational household in 1900, but by 1980 only 17 percent did. Families are increasingly spread out, and numerous studies have found that the frequency of contact be-

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explain how menopause could have evolved was proposed by Steve

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hypothesis posited that the benefits of grandmothers caused nat-

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tween grandparents and grandchildren decreases the farther apart they live from one another.19

If grandmothers were the driving force behind the evolution

of menopause, then these changing family dynamics in industrial societies may be decreasing their evolutionary value. Consistent with this idea and the evidence from Framingham is the observation that the age at which women are experiencing menopause is increasing in many more developed regions. Although the onset of menopause can be related to many factors, including smoking and surgical intervention, the trend suggests that selection on women in industrial societies may be shifting toward a benefit to continued reproduction rather than an end to fertility. Indeed, the rate at which women in their forties and even fifties are having babies has grown, thanks in part to the availability of assisted reproductive technology.20 If all of these trends were to continue over many generations, long enough for there to be a response to selection, future women may cease to experience menopause altogether.

Women are not the only ones having children later in life. In

many developed regions around the world, the average age of fathers has been increasing as well. In Iceland, for example, the average age of fathers went up from twenty-eight to thirty-three between 1980 and 2011. Comparing the complete genomes of Icelandic

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parents and their children showed that fathers pass more mutations to their children than mothers, and the older the father, the more mutations his children receive. This is because, unlike eggs, sperm are continually created throughout a man’s life, meaning that sperm created by older men are made from cells that have divided many times, creating lots of opportunities for mutations to occur. Having more mutations seems to explain at least part of the reason why

and autism, although the genetic causes for these conditions remain population provides more raw material for natural selection, suggesting that these demographic changes may influence the potential for our continuing evolution.

The studies in this chapter illustrate that human evolution has continued into modern times, but the changes that have come with economic development and industrialization have affected the nature and impact that natural selection is having on us. We have so far been limited in what we know about the traits that selection is operating on based on the type of data available—primarily population records and medical studies—neither of which were designed to capture evolutionary changes. But despite these limitations, we can clearly see that the advances we have made in the last few centuries in science, technology, medicine, and overall quality of life have profound implications for the ongoing evolution of our species.

As we move into an era in which more and more human popu-

lations have undergone a demographic transition, we must consider how the increased relevance of selection on fertility—including how we choose our sexual partners and the factors that affect how many children we have—will affect our continuing evolution. In other words, when it comes to the future of our species, there is perhaps no topic more relevant than sex.

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poorly understood.21 But increasing the number of mutations in a

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children of older fathers are more likely to develop schizophrenia

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4 . Sex

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t its core, evolution is about babies. Forget survival of the fittest—the only reason survival is important in evolution is because you cannot reproduce when you’re dead. Ultimately, selection favors whatever traits result in making the most babies, grandbabies, and so on. In human populations that have undergone demo-

graphic transitions (see chapter 3), the vast majority of babies that are born survive until they are old enough to make babies of their own. Babies born in the United States now have a 99.4 percent chance of surviving to celebrate their first birthday and can expect to celebrate about seventy-nine more.1 In such populations, selection

becomes less about the traits that promote survival and more about traits that promote making more babies than your neighbors. Our future evolution, then, has everything to do with sex.

Darwin himself was the first to recognize the importance of

sex and reproduction for the evolutionary process. In The Descent of Man and Selection in Relation to Sex, Darwin not only applied his theory to humans, he also expanded it to include another mechanism for evolutionary change called sexual selection.2 Sexual selection is distinct from natural selection, because sexual selection can result in traits being favored that are not linked to survival.3 The classic example is the elaborate tail feathers of peacocks. It is not hard to imagine 97

how unlikely it is that such a long, gaudy tail would be advantageous for surviving in the wild. Darwin’s insight was to recognize that a trait like the peacock’s tail would be favored if it results in better reproductive outcomes, despite the possibility it might not help prevent death. Since peahens show a preference for mating with males with eyespots on their tail feathers that are brighter and with more iridescent colors that contrast with the surrounding background, males with such characteristics tend to leave more offspring than males without them.4 Peacocks—but not peahens—also have sharp spurs on their legs, not so much to help them to survive but because they are used in battles between males for access to female mates. These two mechanisms— female choice and male-male ­competition—are the bread and butter of sexual selection.

Biologists now believe that the reason females prefer particu-

lar traits in males is that the traits are an indication of the quality of the male’s genes, some of which will be passed on to their offspring if they mate. The message to the peahens seems to be: mate with one of these brightly colored fellows and your babies will hatch as superchicks. That the long, conspicuous tail might be an impediment to the peacock’s longevity may actually be part of the point—Israeli ornithologist Amotz Zahavi noted that the male traits preferred by females are often exactly those that are detrimental to his survival. Zahavi’s idea, known as the handicap principle, suggests that such traits are honest indicators of good genes because males cannot fake these traits without the good genes to back them up.5 A peacock ­attempting to sport a magnificent tail without the physical prowess to escape from predators might not be around long enough

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to mate. Females can therefore be assured that males with traits that essentially handicap them really are genuine.

Another example of females choosing males with traits that

a graduate student, one of my first field research experiences was in Panama, where these frogs are common. We stayed along the canal in former U.S. military barracks now run by the Smithsonian’s Tropical Research Institute. The area had something of a ghost town feel, with block after block of empty streets and abandoned children’s playgrounds being reclaimed by the jungle. After dark, the ­water-filled ditches along the empty roadsides would resonate with the peculiar songs of the little male túngara frogs, adding to the eerie effect.

Behavioral ecologist Mike Ryan has worked with this species

for years and figured out that the calls made by male túngara frogs which, like all frog calls, are used to attract females, actually consist of two parts.6 The first part, called the whine, is a sort of high-pitched squeak that is enough to cause the female túngara frogs to pay attention and maybe even persuade them to mate. But some male túngara frogs add a second part: a low, rumbly chuck that makes their songs sound especially strange—and drives female frogs absolutely wild. It turns out that the chuck part of the call, unfortunately for the ardent males, reverberates around the calling frog and creates a ring of ripples in the surrounding water that is used by frog-eating bats as a way of locating an easy meal. As if that weren’t bad enough for the frogs, the chuck part of the call also attracts blood-sucking flies that feed on the poor male’s nose as he sings. Natural selection alone would not favor a behavior in males that attracts both predators and parasites, but because it leads to better mating success—at least in males who survive long enough to mate—the trait has been favored by sexual selection.

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handicap them comes from the Central American túngara frog. As

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Although researchers like Zahavi, Ryan, and many others have

examined sexual selection in a wide range of animals, we know much less about sexual selection in humans. This situation poses something of a problem for contemplating our future evolution in a world in which selection is primarily about differences in fertility. But we know from studying other species that the two main components of sexual selection are mate choice (which in most species consists of females choosing their male partners) and competition (usually among males) for access to mates. By exploring what we know about these processes in humans, we can piece together a picture of sexual selection that will give us a sense for how selection on the traits that affect reproduction has acted in the past and how it is likely to proceed in the future. ■ The ways that people choose their sexual partners, perhaps not surprisingly, has captured the attention of many people, including a wide range of researchers. Much of the work in this field has been done by psychologists, interested as they are in human behavior.7 The field of evolutionary psychology emerged in the late 1980s and early 1990s as a subdiscipline of psychology, borrowing ideas developed in the 1970s that linked genetics and evolution to behavior. Delving into the evolutionary psychology literature on human mate choice and sexual behavior feels a bit like being a teenager and discovering pornography. It’s exciting, mind opening, and yet—with titles like “Is Cunnilingus-Assisted Orgasm a Male Sperm-Retention Strategy?”— not necessarily something you want to be caught reading. Despite

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the blush factor, evolutionary psychologists have made a lot of pro-



Consider, for instance, how we view other people’s faces. We

make instant judgments about a person’s age, sex, mood, health, and how attractive we find them based on just a quick glance at the face. Psychologist David Perrett has explored in great detail how people perceive faces. When I visited Perrett’s lab one morning in late December, I was caught a bit off guard when I was introduced to a man wearing bright red baggy pants and a fuzzy purple jacket, his long hair dyed green on one side and red on the other. His lab at the University of St Andrews, Scotland, is located just off of St Mary’s quad in the heart of the ancient town of St Andrews, not far from the famous golf course. Contrasted with the solemn formality of the surroundings, Perrett’s appearance could not have been more incongruous. I must admit that for the first twenty minutes or so of our conversation, I could not help but be distracted by the idea that I was somehow part of an experiment, being evaluated by one of the world’s experts on facial perception, to see how I would react to his unusual appearance.

Perrett, who grew up in a small English village near the Welsh

border, was originally trained as a physiologist, and his early research focused on nerve cells, or neurons. He became interested in the astonishing ability of individual neurons to recognize visual patterns and wondered what more complex networks of neurons could do. His curiosity would lead him into the development of tools to determine what cues our brains (which are essentially massive networks of neurons) use when making judgments about a person’s face.

The tools Perrett would develop are, in many ways, a modern

upgrade to a technique that another Englishman stumbled on more

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their sexual partners.

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gress in documenting and explaining how and why people choose

than a hundred years earlier.8 Francis Galton, the Victorian polymath and father of eugenics, was interested in learning whether there were general facial features common to all criminals. The idea that one could discern a person’s character from a careful look at his or her face was prevalent at the time, and if Galton could figure out how criminals looked, perhaps they could be identified prior to committing any crime. To do so, he took photographs of several convicted criminals and developed them on a single photographic plate. The resulting image appeared as a single face that was, in fact, a composite of all of the individual criminal faces. The more faces he included in a single image, the more the resulting face looked less like any one of his photographic subjects and more like an average of them all. To Galton’s frustration, he found no facial features that seemed to typify, say, a murderer or a thief, but he did notice that the composite images appeared more pleasant looking than any of the individual portraits.

Perrett brought the photographic blending technique into the

digital age, using sophisticated computational tools to tweak and sculpt a face on a computer screen in just about any way imaginable. One of the results of this work was strong support for Galton’s observation that blended faces often look better than those of individuals. All else being equal, the research suggests that we find faces to be attractive if their features approximate the average that we have seen in other faces. If nose length, for example, varied in your hometown between four and six centimeters, then you might find a person with a five-centimeter-long nose fairly attractive.

Perrett’s lab was spread across a large room, with computer

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stations along one wall where the study participants would come in and rate faces. Each station had a computer screen with a divider on

taining cameras, tripods, lights, and other photographic equipment for shooting test subjects. Often, Perrett’s subjects are students at the University of St Andrews, but he has included people of different ages, races, and sexual orientations in his search for the general rules for what makes a face attractive.

In addition to averageness, Perrett’s group has also found

that men almost always prefer women with more feminine faces, and women sometimes prefer men with more masculine faces. The sex-specific facial differences that make men look masculine and women look feminine become apparent only after puberty, as the relative amounts of the hormones testosterone and estrogen begin to sculpt male and female faces in distinct ways. Female faces change less than do male faces, and typically have smaller chins and fuller lips. Men’s faces tend to have larger jaws, eyebrow ridges, and are generally wider across the cheeks than women’s. Whether more masculine faces are considered more attractive depends, in part, on who is judging—and when. Women’s preferences for male facial features depend in part on their menstrual cycle. During the fertile phase women tend to find more masculine faces more attractive; at other times, women often find more feminine faces attractive in a man. Preferences also vary depending on whether the woman doing the rating is more interested in a long-term relationship (in which case she would tend to prefer more feminine-faced men) or a shortterm liaison (more masculine faces).

Randy Thornhill, a professor of biology at the University of

New Mexico, has documented a third factor that determines how attractive we consider a face to be. Thornhill became interested in

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ference. An adjoining room looked more like a portrait studio, con-

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either side, shielding the test subject from any outside visual inter-

sexual selection after reading The Descent of Man as a twelve-yearold boy. He grew up in Alabama where, at the time, finding anything written by Darwin was not so easy. He didn’t understand all the details, but he found Darwin’s ideas about how females choose their mates fascinating and highly relevant to his own adolescent interests. Thornhill would go to college, first at Auburn University for his bachelor’s and master’s degrees and then the University of Michigan, where he completed a doctoral thesis on an obscure group of insects known as scorpionflies. He began to notice that some of the genitals of male Japanese scorpionflies were highly asymmetrical, which seemed odd. Once he started looking further he noticed asymmetries in other body parts, too, such as wings. He began designing experiments to see if scorpionflies that differed in how symmetrical they were had other differences, too, and he found they did—females preferred to mate with more symmetrical males, more symmetrical males had better access to female mates, and males and females that were more symmetrical were better at competing for food.

Thornhill wondered whether symmetry mattered in people,

too, and after he met anthropologist Karl Grammer at a conference in Japan, the two began collaborating on the topic. Although others had looked at facial symmetry before, Thornhill and Grammer developed an improved method to determine whether facial symmetry in humans related to how attractive a face was considered to be by a test subject. Their initial study included photos of only sixteen unaltered faces and seven composite photos (images that took several real faces and blended them together), yet the German college stu-

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dents that rated them showed a clear preference for more symmetrical faces in members of the opposite sex.9

Thornhill would go on to partner with psychologist Steven

role of symmetry in human facial attraction and mate choice. Although most real faces are at least somewhat asymmetrical, with, say, a slightly crooked nose or one earlobe just a bit longer than the other, the evidence was overwhelming that more symmetrical faces are considered more attractive. Perrett’s group found this result as well. Using his ability to manipulate digital images, Perrett could keep all facial features the same except for the shape, making it more or less symmetrical. When Perrett’s research subjects were asked to rate how attractive they found a particular face, those that were altered to be more symmetrical were considered more attractive by 60–70 percent of people. Seventy-four percent of his subjects preferred perfectly symmetrical faces, which rarely occur naturally.10

Thornhill and Gangestad conducted detailed surveys of their

study participants, and they began to discover that facial symmetry in men (but not women) correlates with many sexual factors. More symmetrical men tend to be younger when they begin having sex, have more sexual partners, and their female partners achieve orgasm more frequently during sex. Several of their studies have even shown that women can detect the smell of more symmetrical men.11 A typical study works as follows: test subjects are male college students who are asked to wear a new cotton T-shirt for two nights, avoid using any deodorants or artificial perfumes, and avoid smoking or eating any strong-smelling or spicy foods. They then bring the shirts in to the lab where they are given to women (also college students) who are asked to smell them and rate them based on how pleasant, sexy, and intense they find the odor. The men are also photographed, and their faces are scored for symmetry. The results—in addition to

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Gangestad, also at the University of New Mexico, to expand on the

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proving that college students will do nearly anything for credit in an introductory psychology course—reveal that women find the shirts of highly symmetrical men to smell better, and even that the smell is sexier. The preference is strongest among women who do the smell rating during the most fertile phase of their menstrual cycle.

These three components—averageness, sex differences, and

symmetry—explain a lot of the differences between faces that are considered more or less attractive. Perrett explained that other factors can contribute as well (he and his colleagues are currently exploring the importance of color), and he was quick to point out that preferences are not universal. An individual person’s idea of what is and is not attractive will depend, in part, on that person’s visual diet, meaning what he or she saw growing up and what he or she sees on a regular basis. Increasingly, the people we see in our daily lives in the industrialized world—whether in person, in photos, online, on television, or in movies—are a more diverse sample of humanity than was the case in previous generations, when the people around us would have mostly looked similar to ourselves. Not only are we more likely to see people who look different from us, but the people we see, especially in movies and magazines, are often those who are considered particularly attractive. This diversity might be creating biases in our perceptions of averageness and therefore what we consider attractive in others—as well as how attractive we consider ourselves to be.

Facial attractiveness is important for human mate choice, but

we also look at each other’s bodies. Height is widely recognized to be an important element of attractiveness in men. Studies of online dat-

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ing profiles and lonely hearts ads suggest that tallness is among the most common trait mentioned by women seeking men, that taller

vealed that the man is taller in 92.5 percent of heterosexual ­couples.

On average, men tend to be taller than women. In the United

States, men are about 9 percent taller than women, which amounts to about a five-and-a-half-inch height difference.13 Consistent physical differences between the sexes, which biologists refer to as sexual dimorphism, are telltale signs of sexual selection, so perhaps it should come as no surprise that female preference for taller men has led to such a difference. Or, given that a height difference does exist, should we expect men to be taller in most heterosexual couples just because of chance? Interestingly, the U.K. sample accounted for an existing height difference and found there were even more couples with taller men than would be expected by chance if couples were randomly created without regard to height.

Much like a peacock’s tail feathers, these physical features of

a person’s face or body are cues that are used by the opposite sex to get information about the suitability of that individual as a potential mate. Thornhill, Perrett, and their colleagues believe the biological reason for women finding symmetrical men so sexy is that symmetry is established early in development and can get thrown off by just about anything—a slight genetic change, exposure to an infectious disease, or excessive stress are all likely to leave a mark in the form of some sort of asymmetry. Individuals with good genes, the theory goes, can tolerate such abuses and grow symmetrically nonetheless. Choosing a highly symmetrical mate, then, is a way of choosing a good source of genes for your future children. Just like a peacock with a tail full of bright, iridescent eyespots, good genes are a big turn-on.

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sponses to their ads or profiles.12 Data from the United Kingdom re-

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women prefer even taller men, and that taller men get more re-



Likewise, a preference for averageness is explained as a way of

avoiding unusual genetics. A person with an oddly shaped face may have other genetic abnormalities lurking in his or her genome that would best be avoided in your offspring, the logic goes. Preferences for feminine faces in women and masculine faces in men, on the other hand, are thought to be more direct cues related to hormone levels. Because fertility is closely tied with estrogen levels, women with more feminine faces and bodies are, on average, generally more fertile.14 Masculinity in male faces is closely tied to testosterone levels—which also influence height—and testosterone is known to suppress the immune system. Manly-looking men may therefore be displaying the kind of handicap that Zahavi had in mind—flaunting their hormones in the face of all those infectious diseases.

For women, odor can be an important factor in choosing a mate.

Thornhill and Gangestad found that women not only prefer the scent of more symmetrical men, they can also discriminate between the scents of men with immune systems that are more or less similar to their own. Similarity in this case refers to genes in the major histocompatibility complex, the part of the immune system that determines whether something found in the body belongs there or not. A bacterial cell in the blood, for example, might be recognized by the major histocompatibility complex as foreign, triggering an alarm that initiates an immune response. Large differences in major histocompatibility complex proteins between individuals are the primary cause of rejection in organ transplants, since the ­immune system recognizes the new tissue as foreign and attacks it.15 The genes that encode the proteins that constitute the major histocompatibility complex are

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the most diverse in the human ­genome—they have to be to keep up with all the rapidly evolving microbes that cause infectious diseases.

The observation that women can distinguish the major histo-

made by a study conducted in Switzerland, again using university students as subjects.16 In their 1995 paper, Claus Wedekind and colleagues reported that women preferred the smell of T-shirts worn by men with major histocompatibility complex profiles that differed from their own, as determined by a blood test. They suggested that the preference might serve as a way of ensuring that any resulting offspring would have a diverse profile and therefore be more effective at combating infectious disease. It may also help to avoid mating with close relatives, which can increase the risk of birth defects. Their paper kicked off a flurry of follow-up studies as well as some criticisms by researchers who questioned the experimental design. Subsequent laboratory experiments using modified methodologies have mostly supported the idea that women prefer men with dissimilar major histocompatibility complex profiles, though comparisons of profiles of actual couples have so far been inconclusive.17

That people have consistent preferences for physical traits in

their partners suggests sexual selection may be acting to favor traits that are considered attractive in a mate. We have seen evidence that people who are considered more attractive tend to be more sexually active, but how important is being attractive when it comes to what matters most in evolution—making babies? If, for example, men with less symmetrical faces have fewer children than men with more symmetrical faces, then facial symmetry, and hence attractiveness, should become more common in future generations.

Although there has been surprisingly little research on this

question, an intriguing data set from Wisconsin suggests that, at least in some instances, attractive people do indeed have more chil-

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compatibility complex profiles of men based on their scent was first

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dren. Psychologist Markus Jokela used an ongoing multigenerational study of more than ten thousand people that began with a random sample of that state’s high school graduating class of 1957 and subsequently tracked them and their families. Using their old high school yearbook photos, Jokela had judges rate how attractive each person was back in his or her glory days and compared those ratings with data on family sizes. On average, women rated as attractive and very attractive (the highest categories for attractiveness) had 16 percent and 6 percent more children, respectively, than did women in the two lowest attractiveness categories. The least attractive men had 13 percent fewer children than men who were judged to be more ­attractive.18

Taller men, consistently rated as more attractive to women, also

seem to have more children.19 A comparison of family sizes among Polish men undergoing mandatory medical examinations in the 1980s revealed that men with no children at all were shorter on average than men who had at least one child. Even more compelling is a study of the U.S. Military Academy at West Point’s graduating class of 1950, in which taller men were shown to have fathered more children throughout the course of their lives than shorter men, in this case because the taller men remarried more frequently. The West Point study was able to eliminate any differences in career achievement, socioeconomic status, or other variables that are known to correlate with height, suggesting that sexual selection did indeed favor taller men.

Like any trait that has been honed by selection over millennia,

the preferences we have for our sexual partners evolved to increase the number of babies and grandbabies we leave behind. But mod-

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ernization is intervening in this process and may be affecting sexual selection in much the same way as it has affected natural selection.

our partners, and the relationship between sex and making babies.

The initial paper by Wedekind and colleagues that revealed

that women prefer the scent of men with major histocompatibility complex profiles different from their own also uncovered another, perhaps more surprising, result. It turned out that of the forty-nine female study participants, eighteen were taking hormonal contraceptive pills, and they tended to prefer the scent of men who were more similar to themselves in terms of the major histocompatibility complex profile. Subsequent studies comparing the preferences of women on birth control pills with those who are not have shown that their preferences really do change. One study investigated the same women before they began taking the pill and again after they had been on it for a while, concluding that their odor preferences did change. Women on the pill also have different preferences for cues indicative of health and masculinity, and one study showed that women who were on the pill when they met their partner report lower levels of sexual satisfaction in their relationships.20

Hormonal contraceptive pills are the most common form of

birth control in the United States, where more than 80 percent of nonvirgin adult women report having used the pill at some point in their lives. Globally, some 100 million women use the pill, though its use is more common among women in more developed nations. Though access to birth control in less developed regions has improved in recent decades, the World Health Organization estimated in 2015 that an additional 225 million women who would like to use some form of modern contraception, including the pill, still lack ­access.21

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choose our sexual partners, our preferences for the characteristics of

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The changes that have come with modernization affect the way we



The use of hormonal contraceptive pills seems to be altering

the ability of women to utilize the cues that evolved to maximize their reproductive success by changing their preferences in ways that are still being unraveled. Given the importance of odor cues in human mate choice, the widespread use of deodorants and perfumes poses another challenge to our continued ability to differentiate among potential mates. Other cosmetics, including those that alter the color and texture of the skin and lips, may interfere with our abilities to detect cues related to health, age, and hormonal status, which are also important for how we choose our sexual partners.

Another trend affecting human mate choice is the increased

use of the Internet and social media to find sexual partners, including long-term mates.22 So-called online dating has grown rapidly in popularity in the United States where, as of 2013, about 11 percent of adults had tried it. Among those who are single and actively looking for a partner, 38 percent have used an online dating site or mobile app. Among those who use online dating sites, two-thirds end up meeting in person someone they first encountered online, and nearly one-quarter entered into long-term relationships, including marriage. Although it is still more common to meet a long-term partner in more traditional ways, 5 percent of adults currently in long-term relationships met their partner online, and that percentage has doubled in less than a decade. Among people who have been in long-term relationships for ten years or less, 11 percent met online. Given these trends, and the fact that online dating is most common among the youngest generations, it seems that meeting that special someone with the help of technology such as the Internet

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and social media will be even more common in the future.

Online dating has implications for our evolutionary future be-

cial symmetry and averageness are important in determining whom we consider attractive, so seeing someone’s photo on a dating site might allow those factors to continue to be utilized. Odor, on the other hand, could be a factor only once a couple decides to meet in person, so it may be less likely to serve as an initial filter in matechoice decisions.

Online dating may also be changing the mate-choice land-

scape by facilitating contact between people who would otherwise be unlikely to meet. Geographical constraints might still make it unlikely that two people from opposite ends of the Earth will end up together, but it is certainly easier to meet someone outside of one’s own familial, social, and professional circles by tapping into an extensive online network of potential partners.

In this context, I can speak from personal experience. After a

breakup as a graduate student in my midtwenties, I was interested in meeting someone new but didn’t have much time for the usual nightlife scene. Most of the women I knew were fellow graduate students in my program, but I wanted to find someone who wasn’t a biologist like me. So I signed up for an online dating site, struggled to make a profile in which I described my personality and interests as best I could, and found a picture of myself that I thought looked halfway decent. I was thrilled when, after exchanging a few messages, a woman who seemed amazing agreed to meet me for dinner. She was a graduate student at the same university, but in the nursing program on the opposite end of campus. She became my one and only date with someone I met online. Two years later, we were ­married.

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that are used in mate choice. As we have seen, visual cues like fa-

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cause it has the potential to alter the relative importance of cues



Although we were both graduate students at the same school,

the chances we would have met without the aid of an online dating site are low. We had no acquaintances in common, we spent the little free time we had hanging out in different places, and she later told me that she had never even been to the part of campus where I spent most of my time. Even with the help of technology, our first date almost didn’t happen. We had arranged to meet at a restaurant, and I told her I would be wearing a black leather jacket (which I thought looked pretty cool). But the weather forecast changed, and my heavy black jacket seemed like it would be too hot, so I wore a lighter brown jacket instead. I later learned that she arrived early at our designated meeting spot to scope the place out, and as she drove past the restaurant she saw a man standing out front wearing a black jacket that she assumed was me. The trouble was this person was about one hundred pounds heavier than I was, which caught her off guard because she had seen my picture online and expected to be meeting someone slimmer. My weight, she told me, really wasn’t an issue for her, but the idea that I had posted an inaccurate picture of myself was troubling. She wondered what else I might be dishonest about. Luckily for me, she called a friend who convinced her to go on the date anyway. By the time she arrived at the restaurant the mysterious man in black had vanished, in his place a nervous guy in a brown jacket. She was confused at first but recognized my face, and we went on to have the first of many lovely dates.

The perceived dishonesty that almost prevented me from

meeting my wife underscores one of the challenges of online dating —it is very easy to be deceptive. Studies by communication scien-

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tists Jeffrey Hancock and Catalina Toma have revealed that many aspects of online dating profiles are inaccurate.23 Comparing pro-

to be dishonest about their height, whereas women are more likely to lie about their weight. In both cases, the intention behind the dishonesty was to make themselves appear more attractive. Both men and women frequently used photographs that were judged by independent viewers to be inaccurate, either because they were out of date or because the images had been modified or enhanced in some way. Women’s photos were more likely than men’s to be ­misrepresentative.

Profile pictures are critical for success in online dating: profiles

that do not include a photo are seven times less likely to be contacted by a potential partner, and some dating sites use photos alone as a first step in narrowing down the pool. Clearly, it pays to look good. Visual information, however, tends to be more important to men in choosing their heterosexual partners than it is to women. That photos often serve as the first step in mate choice via online dating suggests that this trend might alter the cues evolved by women more than those evolved by men. Unless future technology allows dating websites to incorporate the cues important to women, such as odor, online dating may be yet another way that sexual selection in our ongoing evolution becomes biased toward the interests of men. ■ Our exploration of sexual selection in humans has so far focused on one aspect of sexual selection, mate choice. The other way in which sexual selection operates involves competition over mates. In many species, such as deer, males physically battle one another for access to fertile females. But these competitions do not take place only be-

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their colleagues discovered that men were more likely than women

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files with information collected independently, Hancock, Toma, and

fore mating—they can extend into battles that are played out within the female reproductive tract.

British biologist Geoffrey Parker first recognized this phenom-

enon in the 1960s during his doctoral thesis research at the University of Bristol on the reproductive behavior of dung flies. Parker realized that since female dung flies tend to mate with multiple males in rapid succession, the sperm from those males must be in competition to fertilize her eggs. In a series of papers published in 1970, Parker expanded his basic observation into a general theory of sperm competition and pointed out many implications it could have for the biology of insects.24 His theory explained why many female insects have specialized organs for storing sperm, why in some species males deliver far more sperm than seems necessary for fertilization, and why sperm from one male sometimes create mating plugs to block the entry of sperm from other males. Sperm competition could even be another way for females to screen potential fathers by setting up a contest of sorts in which the most competitive sperm wins. Female mate choice, in other words, does not end with mating but continues until an egg is fertilized.

Parker shared his ideas, even before he published them, with

another young biology graduate student, Robin Baker.25 The two shared an apartment on the outskirts of Bristol, where during cold winter evenings they would huddle around a small gas fire, toasting bread and talking about sex. The pair wondered whether Parker’s ideas about sperm competition might apply to other species—­ perhaps not only insects but also other animals like birds, mammals, and maybe even humans.

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Human sperm competition was fun to discuss, but at the

time it seemed to both young students to be out of reach as a re-

he began to challenge his students to come up with a way to study sperm competition in humans. Years of lecturing would pass before a student named Mark Bellis finally approached Baker with some thoughts on a research approach to the question. The two struck up a collaboration that would lead to some groundbreaking—and ­controversial—findings in human sexual behavior.

To Baker and Bellis, a lot of human sexuality suddenly made

sense when viewed through the lens of sperm competition. In his book Sperm Wars, Baker wrote, “All of our sexual attitudes, emotions, responses and behaviour revolve around sperm warfare, and all human sexual behaviour can be reinterpreted from this new perspective. Thus, most male behaviour is an attempt either to prevent a woman from exposing his sperm to warfare or, if he fails in this, to give his sperm the best chance of winning that warfare. Most female behaviour is an attempt either to outmanoeuvre her partner and other males, or to influence which male’s sperm have the best chance of succeeding in any war that she promotes.”26

Baker and Bellis laid out their argument at length in their 1995

book, Human Sperm Competition: Copulation, Masturbation, and Infidelity.27 Baker and Bellis made the case that evolutionary pressures relating to sperm competition have led to such seemingly unrelated aspects of human sexuality as cheating, masturbation, the shape of the human penis, and the female orgasm, among others. They also offered an explanation for why, out of the roughly 100 million sperm produced in a single ejaculate, as few as 1 percent might be fit for fertilizing an egg. Sperm come in a range of sizes and shapes, including some with multiple heads, multiple tails, or tails that form a spiral,

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versy. When he joined the faculty at the University of Manchester

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search question. Yet Baker was not one to shy away from a contro-

making them poor swimmers. Baker and Bellis concluded that these apparently abnormal sperm might actually be what they called kamikaze sperm, specifically adapted for blocking sperm from other males.

Baker’s lectures were filled with exciting, radical ideas, and

Bellis wasn’t the only young student inspired to pursue the study of sperm competition. Before moving to Manchester, Baker lectured for a time at the University of Newcastle upon Tyne, where Tim Birkhead was an undergraduate student. Intrigued by Baker’s enthusiasm about the new ideas on how sexual selection might extend beyond copulation, Birkhead decided to pursue such research questions in birds. He would go on to become one of the foremost authorities on postcopulatory sexual selection. But, as often happens in academia, Birkhead also became one of his former teacher’s biggest critics. In a review of one of Baker’s books in the popular science magazine New Scientist, Birkhead wrote, “Baker is a sociobiological zealot and uses his book to argue that every facet of procreation, from our behaviour to our anatomy and physiology, is adaptive.”28

Baker and Bellis’s kamikaze sperm hypothesis was especially

criticized, the prevailing view being that misshapen sperm are mistakes rather than the strategic result of an evolutionary arms race. Despite the critics, other researchers, such as evolutionary psychologist Todd Shackelford, have found extensive support for the role of sperm competition in the history of human evolution. Indeed, the aforementioned paper on cunnilingus-assisted orgasm as a male sperm-retention strategy comes from Shackelford and colleagues, who identify oral sex and viewing certain types of pornography as

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among the human sexual behaviors that can be explained in the context of human sperm competition.29

The role of sperm competition in continuing human evolution

ent men to be in direct competition to fertilize an egg. Needless to say, these are difficult data to collect, and surveys of women’s sexual behaviors provide mixed results. Shackelford and his doctoral student Michael Pham point to the approximately 3 percent of children fathered by someone other than the man raising them as evidence that opportunities for sperm competition exist. On the other hand, reproductive ecologists Montserrat Gomendio, Alexander Harcourt, and Eduardo Roldán estimated that women would, on average, have to have sex with a different man every one to three days in order for conditions to favor sperm competition in humans.30

So the role that sperm competition will play in our future evo-

lution will depend in part on our sexual practices, which includes the use of contraception. An intriguing thought is that, much as the overuse of antibiotics promotes the evolution of antibiotic resis­ tance in bacteria, perhaps the increased use of various forms of birth control could put evolutionary pressure on sperm and eggs to evolve countermeasures to increase fertility. In fact, there has been some evidence that female fertility, defined as success in conceiving a child, has been improving in recent decades. For instance, one survey found that between 1982 and 2002, the number of married women in the United States reporting inability to conceive after one year of trying declined by about 1 percent. Likewise, a study of pregnancies in Sweden over a similar time interval found 35 percent fewer cases of below normal fertility for women born in 1975 as compared to those born in 1945.31

Intriguingly, the apparent increase in female fertility comes at

the same time as studies comparing average sperm counts of men in

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will depend in large part on how common it is for sperm from differ-

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different parts of the world that show dramatic declines—from 120 million to 60 million per milliliter—during the twentieth century. Accordingly, the proportion of men with sperm counts in the low range, below 40 million per milliliter, was around 15 percent in the 1930s and had reached 40 percent by the late 1990s. The reasons for declining sperm counts, one of several factors that can contribute to male infertility, are not known. The rapid rate at which they have fallen suggests to some that the cause must be environmental rather than genetic. The mother’s diet and exposure to toxins, especially during pregnancy and for a few months after the child’s birth, are known to correlate with differences in sperm count among adult men. Men whose mothers smoked during pregnancy have been shown to have 20–40 percent lower sperm counts as adults. Exposure to diesel exhaust has similar effects.32 Since the last century, people are increasingly being exposed to a barrage of chemicals for which there is no precedent in our evolutionary history.

Still, genetic causes cannot be ruled out as possible contributors

to declining sperm counts. Some of the genes for sperm production are located on the Y chromosome, which is particularly susceptible to mutations and damage.33 The reason, at least in part, is that one of the DNA repair mechanisms available to most genes is not possible for Y chromosome genes. Most chromosomes exist as pairs, one from the mother and one from the father. Normally, when a gene from one chromosome (say, from the father) is damaged or has a mutation, there is a chance that it can be fixed because there is another copy of the same gene on the matching chromosome (from the mother). Because the Y chromosome does not have a match (its counterpart is

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the X chromosome, which mostly contains different genes than the Y), DNA repair is less effective for Y chromosome genes.

Consequently, genes on the Y chromosome of mammals have

them have lost their function entirely. If that trend continues, as is expected, the Y chromosome could eventually be lost. Such a loss has already happened in some species, such as the mole vole, a fuzzy rodent with impossibly long front teeth. Mole voles still have separate males and females despite having lost their Y chromosome, suggesting that men will not be doomed to extinction once the human Y chromosome fully erodes. The genes that code for male-specific functions like sperm production simply move to other chromosomes. Besides, evidence from fruit flies suggests that the Y chromo­ some doesn’t always fully disappear, since the rate of gene loss in these species seems to slow down substantially once the number of Y chromosome genes becomes very small.34

Modern solutions for the roughly one out of every five couples

experiencing difficulty conceiving have included the development of various treatments for both male and female infertility, artificial insemination, and assisted reproductive technology.35 The latter includes in vitro fertilization, in which an egg is fertilized by sperm in a petri dish and subsequently implanted in the mother’s womb. Just before midnight on July 25, 1978, in Oldham General Hospital near Manchester in the United Kingdom, Louise Brown became the first baby born as a result of in vitro fertilization. Since then, the use of assisted reproductive technology has increased rapidly, and more than 5 million babies worldwide have now been born using in vitro fertilization.

Access to assisted reproductive technology is better in more

developed regions where, as we have seen, birth rates have declined to low levels following demographic transitions.36 Low overall birth

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been in a state of decline for some 300 million years, and many of

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rates and a rise in the frequency of assisted reproductive technology mean that in more developed regions, babies born through in vitro fertilization and other assisted reproductive technologies constitute a growing proportion of the overall population. This trend is amplified by the fact that pregnancies resulting from in vitro fertilization have a much greater incidence of multiple births. In 2011, about half of all in vitro pregnancies in the United States involved twins or trip­ lets, compared to only 3 percent in the general population.37 Indeed, babies conceived in vitro are now estimated to comprise between 1 percent and 5 percent of all births in developed nations, with the highest rates occurring in western Europe. If both trends continue, the total proportion of people in these populations born through assisted reproductive technology will continue to climb.

Many studies have compared the health and well-being of

babies conceived in vitro and those conceived naturally.38 Although some studies have reported differences, the overall pattern seems to be that the health of people conceived through in vitro fertilization is no different than the rest of the population. It may, however, be too soon to know—as of 2015, the oldest are only in their midthirties. We do not yet know whether the children of parents who conceived through in vitro fertilization or other forms of assisted reproductive technology have lower fertility rates themselves. Given that some of the reasons for using in vitro fertilization have a genetic basis, they are likely to be heritable. In other words, in vitro fertilization and other assisted reproductive technologies may be decreasing the strength of natural selection on traits related to fertility.

The first generation of in vitro babies is now at the age at

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which they are becoming parents.39 In 1999, Louise Brown’s younger sister, Natalie Brown, who was also conceived using in vitro fertili-

At least for the Brown sisters, there is no evidence that their parents’ difficulty conceiving has been passed on to the next generation. But of course we cannot draw any conclusions from just one family. It will be another decade or so before it will be possible to know whether there is any difference in fertility between people born as a result of in vitro fertilization and other assisted reproductive technologies and those conceived naturally.

Medical advances continue to provide new options for cou-

ples seeking treatment for infertility. Conversely, new contraceptive methods are providing a range of alternatives to prevent pregnancies. Our species is unusual in that sex has never been exclusively about reproduction, but technology is exaggerating the separation. The extent to which sexual selection will play a prominent role in our future evolution will depend on how far this decoupling extends. Robin Baker, who left academia in 1996 to focus on writing, predicted in his book Sex in the Future that “sex will become almost entirely recreational and reproduction will become almost entirely clinical.”40 He foresees a future in which men and women voluntarily sterilize themselves before reaching sexual maturity, freezing their sperm and eggs for later use in in vitro fertilization. Such a future would eliminate sperm competition as a component of sexual selection, except perhaps for any traits that helped improve the chances of fertilization in the lab.

In a sense, Baker’s is an expanded vision of our reproductive

future foreseen by J. B. S. Haldane in 1924, long before in vitro fertilization was invented. In his book Daedalus; or, Science and the Future, Haldane coined the term ectogenesis to describe the fertilization and

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children and her sister, Louise, has two; all were conceived naturally.

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zation, became the first in vitro baby to give birth. She now has five

growth of an embryo outside the mother’s womb, and in his fictional future it has become universal. Haldane’s idea was borrowed by Aldous Huxley in his 1931 dystopian novel, Brave New World, and by other science fiction authors since.41

But futuristic scenarios like those of Huxley, Haldane, and Baker,

in which technology fundamentally alters the biology of our species, depend on that technology becoming widespread. For contraception and assisted reproductive technology to have a real evolutionary impact on humans, they will need to be ubiquitous, or nearly so. Given the high price of in vitro fertilization, it is currently beyond the reach of many couples even in more developed nations in which the cost is not subsidized. In less developed regions, access to assisted reproductive technologies is quite limited, especially in sub-Saharan Africa, where it is almost nonexistent and yet where some of the highest rates of infertility occur.42 Access to modern contraception is somewhat better, though there are still many regions where it is not readily available, with sub-Saharan Africa again being foremost among them. Widespread access to both would be a great humanitarian achievement—but it might come with an evolutionary catch.

Part of our evolutionary history involved selection on prefer-

ences for our sexual partners and competition among men—or at least their sperm—to become fathers. As with all species, the traits that evolved in our ancestors through sexual selection improved the chances of passing genes on to future generations. Evidence from recent demographic transitions suggests that fertility and sex will be even more important for our future evolution than they have been in the past. But modernization—in the form of online dating, effective

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means of contraception, and assisted reproductive technologies— has once again altered the course of our continuing evolution.

5 . Small Partners

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lthough we might not like to think about it, our bodies are teeming with alien life. Our skin is literally covered with bacteria and fungi and crawling with the tiny legs of microscopic animals. Look inside the average person’s mouth, as any dentist can tell you, and you will find an entire ecosystem dominated by bacteria. Further

down the digestive tract, the stomach—and to an even greater extent the intestine—are veritable microbial jungles.



Until recently, most of these microscopic critters were thought to

fall into one of only two categories: either they were nasty germs that should be killed lest they cause disease or harmless passengers simply along for a ride. The idea that there might be a third category, that some of them might be doing something helpful, seemed like medical blasphemy. An idea that until recently seemed even more ­outrageous—that some of these microorganisms might be not only helpful but an integral part of how our bodies function owing to millions of years of evolving together with us—is only just beginning to emerge.1 If microbes influenced human evolution in the past, then our continuing evolution may depend in part on what becomes of our small partners.

Ironically, with as much as we know about human anatomy

and health, we know far more about how other animals interact with microorganisms than we do about our own intimate associa127

tions with microbes. Many animal species engage in symbioses with microorganisms, without which they could not survive. One example is the leafcutter ants of Central and South America, which depend on fungi as their main source of food.2 They grow enormous gardens of the spongy, gray fungus deep inside their massive underground nests, where millions of worker ants are constantly toiling to bring fresh leaves for their fungal crop. In this case, the fungi have become completely dependent on their ant servants—unlike closely related fungal species that can live on their own, the fungi grown by leafcutter ants are never found outside an ant nest. They have, in other words, become domesticated.

The lab where I undertook my doctoral work at the University

of Texas at Austin, led by Ulrich Mueller, was at the forefront of research on the interactions between ants and microbes. Naturalists and scientists had known for more than one hundred years that leafcutter ants were not eating the leaves themselves but effectively using the fungi as a kind of external digestive system because the ants cannot break down plant matter on their own. Aside from the fungus garden, the rest of the nest was thought to be a relatively sterile environment. The ants are fastidious in their cleanliness, moving unwanted debris, bits of dead fungus, and dead ants to waste chambers kept far away from their precious crops. So it came as a surprise when a Canadian microbiologist, Cameron Currie, who

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joined Mueller’s lab as a postdoctoral researcher around the same time I joined as a graduate student, discovered that another species of fungus was commonly associated with the nests of fungus-­ growing ants.3 The newly discovered fungus was a parasite called Escovopsis, and ant nests with significant amounts of it growing in the garden chambers did not survive for long.

I spent much of my time as a graduate student digging into

leafcutter ant nests, hoping to retrieve a small sample of the funmarauding ants. That is only a slight exaggeration—the mandibles of leafcutter ants, well suited to cutting leaves, can slice through ant can be enough to draw a surprising amount of blood. I quickly learned a technique involving rubber boots and very careful placement of shovel strokes that was mostly effective in preventing such bloodlettings.

Digging into the nests of some leafcutter species, we would

occasionally find worker ants inside the garden chambers that were almost completely white, unlike the typical rust-colored workers commonly seen outside the nest. In other fungus-growing ant species, a small patch of white could be seen under the ant’s neck. Currie learned that the white patch was actually a coating of bacteria growing on the outside of the ants’ bodies. But unlike the parasitic fungus he had discovered, these bacteria did not seem to be harmful to the ants. Instead, they actually seemed to be preventing disease by producing antibiotics that kept fungal pathogens such as Escovopsis at bay.4

These ants are interacting with at least three different types

of microorganisms—the fungus they grow as food, the other fungus that causes disease, and the bacteria that prevent the disease—each of which has a major impact on the health and well-being of the colony. What’s more, there was strong evidence that the ants share a long history with all of these microbes, and that both types of fungus and perhaps also the bacteria have evolved along with the ants in a kind of evolutionary dance—as one species changes, the others

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human skin with equal ease, and one pinch from a large soldier

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gus garden for genetic analysis before being chewed to pieces by the

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change along with it. After millions of years, this creates a pattern of relatedness between species of ants that closely matches the patterns of relatedness among the microbes.5 Biologists call this process coevolution.

As fascinating as the leafcutter symbiosis is, it is not all that

unusual. We now know of many examples of complex interactions between animals and microbes: plant-sucking aphids rely on symbiotic bacteria to provide the nutrients lacking in their vegetarian diets; coral rely on microscopic algae to turn sunlight into energy; bobtail squid use light-producing bacteria housed in specialized organs as a form of camouflage. There are so many of these amazing interactions, in fact, that these symbioses are now seen as the rule rather than the exception.6 The more we look, the more we find that these are often ancient relationships—arms races between enemies and shifting alliances among partners played out over millennia.

Applying the lessons we have learned from other species to

ourselves, however, has taken time. Ever since we discovered that microbes are to blame for infectious diseases, we seem to have been on a mission to try to destroy pretty much all of them. First came vaccines and then antibiotics, followed more recently by antimicrobial soaps and hand sanitizers, which seem to have become almost ubiquitous in more developed, urban regions. We not only try our best to kill any microbes living in and on our bodies, we also attempt

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to sterilize our environments. Our homes, offices, and schools are scrubbed, wiped, and doused with chemicals meant to leave no microbial survivors. We have declared war on microorganisms.

In some ways, our efforts have paid off. We eliminated once-

common diseases including smallpox, and others—such as cholera and tuberculosis—are now mostly confined to less developed re-

amazing declines in death rates, driven in large part by much lower demographic transition.

The trouble is, we are slowly beginning to recognize that not

beneficial or even necessary. As is true for other animal species, many of these microbes have been with us for millions of years and have become so specialized that they can be found nowhere else on Earth except the human body. They have been our coevolutionary partners, and if our war on microbes is successful, they may soon become extinct. Losing our ancient companions might have catastrophic consequences for our future. ■ A short walk from the red line of the Washington, D.C., Metro in Rockville, Maryland, is the extramural funding office of the National Human Genome Research Institute, part of the National Institutes of Health. On the fourth floor of an unassuming redbrick office building, I met Lita Proctor, the person responsible for overseeing the distribution of about $200 million in federal government research funding. Trained as a microbial ecologist, she was a professor at Florida State University and the University of California early in her career. She later worked as a program officer at the National Science Foundation before joining the National Human Genome Research Institute in 2010. This was the branch of the National Institutes of Health responsible for sequencing the human genome and the International HapMap Project. Now, Proctor explained, the National Institutes of Health was working on a new project that was, in many

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all microbes are bad for us. Some, we are starting to learn, can be

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rates of childhood mortality, which are a major component of the

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gions. These microbial persecutions are largely responsible for the

ways, far more ambitious—rather than describing the full DNA sequence of just a single species, researchers were after humanity’s entire microbial entourage.

In the early 2000s, just as the first human genomes were

being published, there were already rumblings that the next major genomics initiative should focus on the microbes associated with the human body. In 2001, a term was suggested by molecular biologist and Nobel laureate Joshua Lederberg to describe all those microbes that we live in intimate associations with—the human micro­biome.7 Microbiologist and biotech pioneer Julian Davies wrote a letter to the journal Science, published in March 2001, arguing that efforts aimed at understanding human biology that ignore the micro­biome might be overlooking a significant factor in human health. He pointed out that although there were thought to be about thirty thousand genes in the human genome, there were probably more than a thousand microbial species ( just a ballpark estimate, because no one really knew how many there were) that constitute the human microbiome, and these might contain as many as 4 million genes that contribute to our well-being.8

A meeting in Paris in October 2005 attempted to organize ef-

forts by researchers around the world interested in investigating the human microbiome. Next-generation sequencing technology had just been developed, and there was hope that the shotgun approach

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could overcome one of the largest obstacles in studying microbial diversity. Whereas classical microbiological techniques began with taking a sample of some unknown microbe and attempting to grow it in a petri dish so it could be studied, it became apparent starting in the 1970s that these methods were missing large and ­interesting portions of the microbial world.9 Quite a few microorganisms—

gun sequencing could, it was thought, bypass the petri dish stage whatever was in them.

After the Paris meetings, the National Institutes of Health held

scale. The Human Genome Project had ended, and one of its primary goals—to improve human health—had not yet been achieved. This was in part because, although we had learned a significant amount about our own genetics, we still knew comparatively little about the organisms that make us sick. Exploring the microbiome, which contains those disease-causing organisms and many more, might provide the missing clues.10

The Human Microbiome Project was launched in 2008 with

a budget of $175 million for the first phase. Its initial goal was essentially to conduct an inventory of the microbial species living in and on the body of a healthy person, the so-called core microbiome. Researchers would focus on five main parts of the body—the skin, mouth, upper airways, intestine, and vagina. This inventory of core species could then be compared with the list of species found on people suffering from various infectious and noninfectious diseases. Any discrepancies between these lists might be clues to the causes of some of the mysterious conditions, such as autoimmune disorders, that were becoming more common.

Dozens of research labs funded by the Human Microbiome

Project began collecting samples from volunteers. The shotgun sequencing approach worked, but it quickly became clear that the idea of a core microbiome was fundamentally flawed. A paper published in 2012 summarized the overall results to date: every person sam-

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its own meetings to consider funding microbiome research on a large

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entirely, extracting DNA directly from the samples and sequencing

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entire categories of them—simply wouldn’t grow in the lab. Shot-

pled was host to a different set of microorganisms, and the species that did show up consistently were common in some people but rare in others.11 Rather than describing the one set of microbial species that characterize all healthy human bodies, the emerging picture of the human microbiome was one of individual differences.

Nevertheless, there were some striking patterns. In much the

same way that habitats such as deserts, rainforests, and grasslands contain predictably different types of plants and animals, the different parts of the body housed distinct communities of microbes. As expected, the digestive tract, including both the mouth and the intestine, had the greatest microbial diversity. Interestingly, the mouth had a lot of different types of microbes, but most people’s mouths tended to have the same types. The vagina showed the opposite pattern—its microbial diversity was low, and people varied quite a bit in the types that were present. By sampling the same individuals twice, researchers also discovered that the types of microbes present change through time. Yet despite some fluctuations, individual people seemed to have a characteristic microbiome that is unique.

Some of the differences between the microbiomes of differ-

ent people seemed to be due to environmental factors such as diet. Vegetarians, for instance, have somewhat different microbes living in their guts than do meat eaters or people with high-carbohydrate diets. Such differences might explain why people from different cul-

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tures tend to have different microbiomes (they eat different foods) and why family members tend to have more similar microbiomes (they eat similar foods). But there was also evidence suggesting a genetic component to the differences between people’s micro­biomes.12 A study comparing the microbiomes of identical and fraternal twins, both of which presumably share the same household envi-

were more similar than the microbiomes of fraternal twins. Because ternal twins share about half of their genes, the differences in the micro­biomes seemed to be due primarily to differences in their

The question remained whether our microbes, and the com-

munities that they form in different parts of our bodies, are unique to humans. If not—if the same microbial communities could be found in, for example, the gut of a gorilla and the gut of a human—then there would be no reason to believe that our microbiome evolved along with us. If, on the other hand, there is something special about the human microbiome that makes our microbes distinctive from those of our closest relatives, then it would be worthwhile considering our coevolutionary history—and future.

Sampling the microbiome of wild apes is not quite as easy

as sampling microbes from people, but luckily a lot can be learned about what lives in the gut from examining feces. A group led by evolutionary biologist Howard Ochman did just that, extracting DNA from fecal samples taken from wild chimpanzees, bonobos, and gorillas, which the researchers sequenced and compared with fecal samples taken from people living in urban and rural parts of Africa and other continents.

The results suggested that our gut microbial communities are

substantially different from those of our closest primate relatives.13 The most obvious differences were in the levels of diversity of microbes found in apes as compared with different human populations. All humans had significantly less microbial diversity in their guts than did the nonhuman species, and among the human pop-

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genomes.

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identical twins have almost exactly the same genome whereas fra-

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ronments and diets, found that the microbiomes of identical twins

ulations, those living in urban environments had less diversity than people living in rural areas.

Humans and apes also differed in how common the different

microbial groups were within their guts. Apes had a more even distribution of the different types of microbes. In most human guts, on the other hand, just a few types of bacteria predominated, whereas others were present in low numbers. When Ochman and his colleagues compared the frequency with which different microbial groups were found within a particular species, they found that the more closely related individual hosts were, the more similar were their gut communities. This pattern applied not only within species but between them as well. Ochman and his colleagues used these data to create two family trees, one for the gut microbial communities and another for their ape hosts. The ape tree showed how each species is related to one another based on DNA sequences—the more closely related any two species were, the more branches they shared on the tree. On the gut microbe tree, more similar microbial communities shared more branches on the tree. The two trees looked nearly identical.

Ochman and his colleagues concluded from their data that

ape and human gut microbiomes evolved along with their hosts, and that the human gut microbiome in particular has changed substantially over the last several million years. Here was evidence for

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the type of coevolutionary dance between microbes and their hosts known to be common in other species. As in all good dances, co­ evolution requires that each partner respond to the other. It seems our microbes have been evolving in response to us, and so we may very well be evolving in response to them. We do not yet know. As Lita Proctor explained to me, the field of human microbiome re-

But by the end of the first phase of the Human Microbiome Project researchers in a wide range of disciplines were clamoring to find ways to include it in their studies.

In 2008, a Venezuelan army patrol helicopter flying over a remote region of Amazonian rainforest spotted a collection of huts that did not appear on any maps. This was the territory of the Yanomami, an indigenous group that lives a traditional hunter-gatherer lifestyle in the rugged jungle region spanning the Venezuelan border with Brazil, some of whose members remain isolated from the outside world. The following year, a medical team returned to the site, becoming the first non-Yanomami to make contact with the villagers.14 Before providing vaccinations and antibiotics to those who needed them, the medical team swabbed the skin and mouths and took fecal samples from thirty-four of the fifty-four villagers and preserved them in liquid nitrogen.

When the microbial genome sequences were analyzed, the lead

researcher, Maria Gloria Dominguez-Bello, was amazed. The samples contained the highest diversity of gut microbes ever recorded from humans. Dominguez-Bello, who was born in Venezuela and studied micro­biology in the United Kingdom, had looked at micro­biome profiles of isolated people before. The results had been similar— research by her team and others consistently found that people in more rural environments had more diversity than ­urbanites—but the Yanomami, without previous contact with outsiders, had an extremely different microbiome.15 The further removed people are

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■

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in 2012, human microbiome research had became a hot topic, and

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search is too new, and there are still more questions than answers.

from industrialization, the data suggested, the greater the microbial diversity in their guts.

To put it another way, urban Westerners have the lowest diver-

sity of gut microbes of any people on Earth. If our bodies are habitats for microbes in the same way that forests and grasslands are habitats for plants and animals, then these differences in diversity may be important. Ecologists have found that more biologically diverse habitats are more functional and also more resilient in the face of change, suggesting that low-diversity environments can be unstable. Although less is known about microbial communities, some studies have shown that declines in bacterial community diversity resulted in decreased functionality in ways that parallel the ­better-known plant and animal communities.16 Modernization, it would seem, has left a mark on the ecosystem inside our bodies.

Inhabitants of less developed regions not only consistently

harbor a greater diversity of gut microbes, they also have gut micro­ bial communities that are different in composition. Parasitic helminths, including roundworms, whipworms, and hookworms, are extremely common among people in areas with poor sanitation, where the eggs from these parasites develop in the soil and are ingested or enter the skin of the feet when people walk barefoot. The particular types of bacteria residing in the gut are also different. One type of bacteria, known as Treponema, is consistently found in

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the guts of people living traditional lifestyles, both in South America and in Africa, but absent from Westerners. Treponema had also been found in the guts of wild apes, suggesting they may have been present in our ancestors. A study led by anthropologist Cecil Lewis of the University of Oklahoma found at least five different species of Treponema in the guts of traditional people that have never been

species with their close relatives found in other hosts suggested they

Even among microbes that show up in the guts of urban West-

erners and those living agricultural and traditional lifestyles, there are. Another type of bacteria, Prevotella, which are also thought to facilitate digestion of a diet high in fiber and complex carbohydrates, are common in the guts of traditional people but rare in urban Westerners. In contrast, urban Westerners tend to have a lot more bacteria in the genus Bacteroides—consisting of as much as a quarter of the microbial species in the intestine—than do people living traditional lifestyles.

Comparing people alive today living traditional versus urban

industrial lifestyles certainly seems to suggest that urban Westerners have lost a lot of the microbial diversity once present in our ancestors, quite possibly including microbes that coevolved along with us. But modern people living traditional lifestyles are still modern people. They have had as much time as the rest of us to evolve, and although their way of life may resemble that of our ancestors, their biology might not. To really know what the microbiomes of ancient people were like, we would somehow need to sample them directly.

By 2006, major improvements had been made in the study of

ancient DNA, led in large part by Svante Pääbo’s group at the Max Planck Institute for Evolutionary Anthropology in Leipzig, Germany. One of the biggest obstacles to retrieving human DNA from ancient bones had been contamination by both modern human DNA and DNA from microbes.18 Although researchers had mostly overcome the issue by establishing clean rooms such as the one I saw at David

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are potentially important differences in how common certain groups

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may play a role in digesting complex carbohydrates.

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seen in people living urban, industrial lifestyles.17 Comparing these

Reich’s laboratory at Harvard, it occurred to some scientists, including Cecil Lewis, that the contamination problem might have a silver lining.

Lewis was a postdoc around the time that Pääbo, Reich, and

their colleagues began publishing the first Neanderthal genomes. Next-generation sequencing was brand new, and the Human Micro­ biome Project was about to begin. Lewis saw his chance to carve out a research niche by looking at ancient human microbiomes. The trouble was microbial communities can change quickly—just think about what happens to a piece of fruit left out on the kitchen counter too long. Surely any microbes found associated with human remains thousands of years later would bear little resemblance to the microbes that once inhabited that same body when it was alive— unless they were extremely well preserved. Although an Italian group had had some success in sequencing microbial DNA from the five-thousand-year-old frozen remains of a man found preserved in a glacier high in the Alps known as Ötzi the Iceman, there were very few other examples of such fortunate circumstances.19

Luckily, two other reliable sources of microbial DNA from an-

cient humans were discovered, originating from opposite ends of the digestive tract. Teeth are among the most commonly found ancient remains, and they often have a hard coating of dental plaque and calculus—the stuff that dental hygienists scrape away with those

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sharp metal hooks—formed by bacteria living on their surface. In the absence of modern hygiene and professional dental care, plaque and calculus slowly accumulate over a person’s lifetime, leaving a trea­ sure trove of bacterial DNA. Examining human dental remains from central Europe and the British Isles that ranged in age from preagricultural to medieval, a team led by Alan Cooper, New Zealand–born

nities underwent dramatic shifts after the development of agriculmicrobial diversity declined, bacteria known to cause dental cavities and periodontal disease become more common, and bacteria associ

But the oral microbiome is not the same as the microbiome of

the gut. Just as the Human Microbiome Project was beginning, Lewis was working with another source of microbial DNA from ancient humans in preserved feces, known as coprolites. According to Lewis, coprolites look a lot like recently formed human feces—minus the smell. And under the right circumstances, like when they are left in cold, dry caves, they can still retain much of the microbial DNA they had when they were first deposited. Lewis and his colleagues were fortunate enough to find two well-preserved human coprolites in a cave in Durango, Mexico, that were approximately thirteen hundred years old. In Lewis’s new lab at the University of Oklahoma, he and his colleagues extracted DNA and used a shotgun sequencing technique to analyze the coprolite microbial diversity. They then compared the results to microbial profiles of fecal samples from modern humans as well as to microbes found in soil and other possible sources of contamination.21 Luckily, contamination could be ruled out—the bacterial communities largely resembled those found in the guts of modern humans, particularly those living in rural environments. Just as in modern hunter-gatherers, they found a high prevalence of Treponema and Prevotella. In fact, the overall profile was a better match to modern people living in rural environments than it was to urban-dwelling Westerners.

So direct comparisons between the microbiomes of ancient

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ated with good health declined.

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ture and again after the Industrial Revolution.20 In both transitions,

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researcher of ancient DNA, found that the oral microbial commu-

and modern people showed the same patterns as comparisons between modern people living traditional versus industrialized urban lifestyles—modern urbanites have lost a significant amount of microbial diversity, and some of the missing species might have been beneficial. Major changes in diet certainly seemed to be one of the likely reasons for the changes in our oral and gut microbiomes, but there are plenty of other ways in which the modern urban lifestyle may have affected them.

Improvements in sanitation and especially in water quality be-

ginning in the late nineteenth century certainly played a large role in minimizing the number of microbes to which city-dwellers were exposed. Waterborne diseases such as cholera were dramatically reduced following the widespread treatment of water with chemicals such as chlorine that act as disinfectants. These improvements probably also impacted the ability of beneficial microbes that inhabit the human body to be spread from one person to another.

But as far as we know, people acquire much of their micro-

biomes from their mothers. Many of these are transferred from mother to baby during birth, as the baby passes through the vagina and also comes into contact with microbes from the mother’s skin and anus. But Cesarean sections—in which the baby is surgically removed from the mother’s abdomen—are becoming increasingly common around the world: in Brazil, nearly half of all babies are born via Cesarean section; nearly one-third in Australia and the United 142

for saving many lives, but they limit the possibilities for a baby to ac-

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procedure, Cesarean sections are generally safe and are responsible

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States; and about one-quarter in Canada and China.22 As a medical

quire its mother’s microbes. To make matters worse, at least as far as acquiring beneficial microbes go, many women are given antibiotics

that the baby is exposed to any living microbes. Clean drinking water and sterilization of the birth process have

been powerful weapons in our war on microbes, but it was the discovery of antibiotics in the twentieth century that gave us our mefirst antibiotic (penicillin) in 1928, when he noted its ability to control bacterial growth in petri dishes, he wasn’t able to find a way to successfully use it to treat patients with bacterial infections. Another type of antibiotic, a sulfonamide, was discovered a few years later by German biochemist Gerhard Domagk that proved to be effective on people—including his own daughter, whom he successfully treated for a serious infection during the early stages of his research.23

Unfortunately, the sulfonamides were effective only against

some types of infections. Given that more people had died from disease than in combat in World War I, the start of the Second World War created a new urgency for finding a more consistently useful antibiotic. Fleming’s original discovery of penicillin produced by bread molds would finally prove useful. Following his lead, a team of British researchers isolated a strain of penicillin from a moldy cantaloupe found in Peoria, Illinois, in 1943 that could be mass-produced and was incredibly effective. Other antibiotics, such as tetracycline, were soon developed and deployed to devastating effect on our microbial enemies. Common diseases such as tuberculosis and scarlet fever that killed people—especially children—by the thousands were finally under our control. The war on microbes was in full swing, and it looked as if we were winning.

The good thing about the new antibiotics was that they were

effective against a wide range of bacterial infections, but they also

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dicinal nuclear weapon. Although Alexander Fleming discovered the

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during childbirth, even for vaginal deliveries, making it very unlikely

killed lots of different types of bacteria, not just those causing an infection. As biologist and science writer Rob Dunn has stated, “The question is not whether our antibiotics, in the most general use of the term, have helped us, but instead, when we pull the trigger, how well we are able to aim.”24

Among the many casualties were microbes that have been

with us for ages—our coevolved partners. Helicobacter pylori is one of these. It lives in the thick layer of mucus that lines the inside of the stomach, one of the few microbes that can tolerate the extreme acidity there. Its relationship with its human hosts is complicated, because H. pylori has something of a Dr. Jekyll and Mr. Hyde personality. It has been linked to stomach ulcers and cancer, yet a growing body of evidence suggests that people who do not have it in their stomachs are more susceptible to other ailments, including chronic gastric reflux and asthma.25 This is a species that has been with us for at least one hundred thousand years.26 It was our companion as we spread out of Africa, joining those pioneers who settled nearly every corner of the globe. It has come to depend on us, being unable to live outside the human body. But it is disappearing.

At the beginning of the twentieth century, most people

around the world had a colony of H. pylori growing in their stomachs. By the end of the century, fewer than half of adults in more developed ­regions had it, and far fewer children. Babies are not born with

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H. pylori and, as it is a bacterium that grows only in the human stomach, the only way to acquire it is from someone else during childhood, usually from the mother or another family member. A study led by American medical doctor and infectious disease researcher Martin Blaser found that among children born between 2002 and 2006 in the Dutch city of Rotterdam, 75 percent fewer of them had

ible decline in just one generation. Fewer than 6 percent of children percent of children in Japan born after 2010 did.

Blaser believes that H. pylori may serve as a sort of microbial

our microbiome. Early in his career, Blaser worked as an infectious disease surveillance officer at the Centers for Disease Control and Prevention before taking an academic position at the University of Colorado, where his lab began to focus on the role of bacteria in the stomach. Australian physicians Barry Marshall and Robin Warren discovered H. pylori in the early 1980s and demonstrated—through an experiment Marshall conducted on himself—that killing it could cure gastritis. Marshall and Warren went on to show that H. pylori was also responsible for ulcers, and Blaser found that it was associated with stomach cancer.28 It seemed clear to everyone, including Blaser, that H. pylori is bad for human health and that people who have it should be treated with antibiotics.

But subsequent work in his lab, which relocated first to Van-

derbilt University and later to New York University, caused Blaser to reconsider this view. By helping to regulate the production of stomach acid, Blaser’s work suggested, H. pylori actually prevents chronic acid reflux and cancer of the esophagus. What’s more, he found that H. pylori can communicate with the body’s immune system through specialized cells that line the stomach and seem to play a role in preventing allergies and asthma. In the war on microbes, Blaser went from being one of the foremost leaders in the battle against stomach bacteria to an outspoken advocate for a more nuanced view of their role in human health.

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early-warning system, giving us insight into what is happening to

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born in the United States after 1995 had H. pylori, and fewer than 2

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H. pylori in their stomachs than did their mothers.27 It was an incred-



In his 2014 book Missing Microbes, Blaser made the case that

our excessive use of antibiotics in the last half century is at least partly responsible for many of what he calls modern plagues—­ conditions such as asthma, food allergies, and cancer, which his research linked to H. pylori—as well as others, such as obesity. It is noteworthy that these modern plagues began to rise in the second half of the twentieth century, around the same time that infectious diseases such as tuberculosis, measles, and hepatitis A underwent rapid declines.29 According to Dominguez-Bello—the Venezuelan micro­biome researcher, who is also Blaser’s spouse—food allergies, asthma, and other modern plagues are unheard of among people living traditional lifestyles like the Yanomami, who all have H. pylori in their stomachs.

A comparison of children who were treated with antibiotics

as babies revealed that they became heavier than those who did not. Likewise, children born via Cesarean section—who presumably were not exposed to many of their mothers’ microbes during birth— are more likely to become obese than children born vaginally. They are also more likely to develop asthma and certain allergies. Experiments on mice showed that treatment with antibiotics made them gain weight. Mice fed a high-fat diet also gained weight, but those with both a high-fat diet and antibiotics gained excessive amounts of weight.30 This effect is well known in the agricultural world—­

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livestock are often fed antibiotics to enhance their growth—and the same principle seems to apply to people.

Obesity has become a global epidemic, leading to health prob-

lems ranging from cardiovascular disease to diabetes. So if antibiotic use leads to excess weight gain, it could also indirectly be responsible for many other conditions. But Blaser also sees evidence for

unrelated afflictions as food allergies, eczema, hay fever, celiac discommon in more developed regions. In all cases, Blaser argues, gut microbes play a role in maintaining normal functionality, and killing

Not everyone has been convinced by Blaser’s arguments, es-

pecially in the medical establishment. From his office in the massive Michael E. DeBakey Veterans Administration Medical Center in Houston, Texas, David Graham explained to me why he is skeptical. “We’re in a bullshit era,” he told me. “We’re a long way away from having what I would call reliable data. We’re in a kind of fun stage where you can publish anything that you do and make big claims for it.” Graham, a practicing gastroenterologist who has also studied H. pylori and other bacteria and their role in human health, remains convinced that they should primarily be viewed as agents of disease. In response to one of Blaser’s articles, Graham wrote a reply entitled “The Only Good Helicobacter pylori Is a Dead Helicobacter pylori,” a view that seems to represent the mantra of the medical establishment on this particular species of gut microbe.31

Yet the general idea that some of our gut microbes can be

beneficial is catching on. Probiotics—foods and dietary supplements that include live cultures of bacteria like Lactobacillus—have been popular for many years in Japan, and are growing in popularity in Europe and North America.32 Likewise, an emerging treatment for the vexing problem of infection with the bacteria Clostridium difficile involves transplanting a sample of feces from a healthy person directly into the patient’s colon. The procedure has been very successful, presumably because of the positive effect of the donor’s microbes

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them with antibiotics throws the whole system out of whack.

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ease, and inflammatory bowel disease, all of which are increasingly

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more direct connections between antibiotic use and such seemingly

in combatting the infection, yet the exact species responsible for the benefit are not yet known.

Research on the human microbiome is still in its infancy, and

the field is moving fast. But the more we learn, the more it seems that the changes our species has experienced in the last ten thousand years, beginning with the development of agriculture and proceeding through the Industrial Revolution, have had major effects on our coevolved microbes. The available evidence suggests that those of us living in modern urban centers have microbiomes that are the most different—both in terms of diversity and the presence of particular species—from those of our ancestors. We do not yet know how many of the microbes that live in such intimate associations with us are harmful, helpful, or just along for the ride. A considerable amount of evidence suggests that some autoimmune disorders, including Type-1 Diabetes and Crohn’s disease, are linked to the current lack of helminth worms, whose presence seems to help our immune systems from overreacting.33 Species such as H. pylori, Treponema, and Prevotella are among the first bacteria from our gut microbiome to be examined in much detail, and they seem to suggest that as the world becomes more developed, urbanized, and reliant on antibiotics and Cesarean sections, we are on the verge of completely eliminating species that have coevolved with us for millennia.

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■ We do not yet know the implications for our evolutionary future of losing our long-term partners. The best way to answer this question may be to look at what happens to other animals when they lose their microbial partners. Coral, for instance, have depended for millennia on microscopic algae called Symbiodinium that engage

share with their coral hosts.34 If conditions are not optimal—such as in recent years—the Symbiodinium can leave a coral colony, resulting in bleaching, which may result in the death of the coral. Termites also depend on coevolved microbes for nutrition.

Credit for their infamous ability to eat wood should actually be given to the billions of microbes, including bacteria and others, living in their guts. There are so many of these beneficial microbes, in fact, that they make up about 40 percent of the weight of the average termite. Experimental treatments in which termite queens were given anti­biotics that targeted bacteria reduced the survival and reproductive success of the queens and, by extension, the entire termite ­colony.35

Mice and other animals can be kept microbe-free by perform-

ing Cesarean sections under sterile conditions and then raising them inside carefully controlled environments supplied with sterilized food and water. Comparing microbe-free mice and rabbits with mice and rabbits that are born and housed in standard conditions suggests that the complete elimination of the microbiome causes changes to the animal’s ability to extract energy and nutrients from its food, process waste products, develop functional immune and nervous systems, and even affects its behavior.36 Normal mammalian development depends on having an intact microbiome.

The more we learn about the many roles of our microbial part-

ners, the more it becomes clear that part of our evolutionary history involved outsourcing—some of the jobs that could be done in-house, by our own genes, are instead performed by the genes present in our microbial partners. This is an advantageous arrangement, in part

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when water temperatures rapidly rise, as has happened repeatedly

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in photosynthesis, turning sunlight into chemical energy that they

because our microbiome contains one hundred times more microbial genes than does our own genome, meaning our partners can perform far more functions than we can on our own.37

Some have even gone so far as to argue that we should aban-

don the old concept of distinguishing between an animal (or plant) host and its microbial symbionts. Instead, this new view, known as the hologenome theory, suggests that the host and symbiont should be considered together as a collective unit, or holobiont, that is capable of evolutionary change.38 One of the implications of the ho­ logenome theory is that whereas our own genomes are more or less static—we are pretty much stuck with the genes we were given at conception—our microbiome is dynamic, able to change its composition in just a matter of days. That suggests that microbial species with genes that are capable of different tasks—protection from a particular type of infectious bacteria, for example—could be acquired that confer benefits to the host-microbe collective. Perhaps more important, our microbiome can evolve far faster than we can— about one hundred thousand bacterial generations for every one human generation. That means that in addition to swapping out one type of microbe for another, the microbes that remain with a particular host over many generations can quickly adapt as environments change.

We need that versatility—conditions are changing more rap-

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idly for people today than ever before in our history. Our diets are undergoing substantial changes as processed foods high in calories and fat replace the more traditional high-fiber, low-calorie diets of our ancestors. Infectious diseases have always been important players in our evolutionary history, as we saw in chapter 1, and the combination of our massive population size and global transportation network

are exposing ourselves to new, potentially harmful microbes more fewer tools with which to combat them. Like all ecosystems, our bodies work better when they are filled with a diversity of life, especially

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species that have been there, evolving, for millennia.

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frequently while extinguishing our microbial partners, giving us

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makes us especially susceptible to the spread of new diseases. We

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6 . Beyond the Horizon

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O

ur discussion of the future of our species so far has looked at what we know about our evolutionary history as well as recent trends so that we might peek into our evolutionary future. We have seen how our large population size and global transportation networks influence both the diversity of our gene pool

and our susceptibility to infectious diseases, and how those diseases are likely to continue to act as agents of natural selection. We have looked at other ways in which natural selection has affected us, and how selection changes as economic development leads to demographic transitions. And in regions that have undergone demographic transitions, we have seen how sexual selection and the disappearance of our microbial partners may play more prominent roles in our evolutionary future. So far, though, our discussion has mostly looked into our relative short-term future—the next thousand generations or so.



What are the long-term prospects for our species? Will we

eventually become extinct, or will we remain more or less the way we are now, with just minor tweaks to our genes and microbes? Or will we, like so many species before us, evolve into another type of organism—a new species of human? Just what can we say about the ultimate fate of Homo sapiens? 155



Statistically speaking, the odds really aren’t in our favor. Based

on what we know from the fossil record, 99.99 percent of species that ever lived have become extinct. As writer Bill Bryson put it, “We come from a planet that is very good at promoting life but even better at extinguishing it.”1 Extinction can happen at any time. There have already been five instances in the history of our planet in which an event that was both catastrophic and global in scope triggered widespread death on a massive scale. The most devastating occurred about 250 million years ago, ending the Permian era, possibly following the eruption of a supervolcano in Siberia. Somewhere between 80 and 95 percent of all species alive at the time were wiped out entirely. Another mass extinction 65 million years ago was almost certainly due to the impact of a six-mile-wide asteroid that struck Mexico’s Yucatán peninsula, killing the dinosaurs and a great many other species as well.2

Such events could happen again. Eventually, they will happen

again. Based on the number, size, and age of impact craters that have been found on Earth, researchers estimate that meteors the size of the one that killed the dinosaurs hit the Earth about every 80 million years.3 The last impact was 65 million years ago. But if humans are still around when the next one comes, we should not be as caught by surprise as the dinosaurs presumably were, given that we are able

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to monitor the movements of asteroids in space and predict their future trajectories.

NASA already monitors asteroids within our neighborhood, or

so-called near-Earth objects. Thanks to these efforts, we know that an asteroid about two-thirds of a mile wide—the length of twelve football fields—will come fairly close to Earth on March 16, 2880. NASA scientists think there is no more than a 0.33 percent chance

than three miles deep if it struck land, or if it hit the ocean, a tsunami with waves several hundred feet high.4 Quite a few methods oid that we know is headed our way: from deflecting it by crashing a spacecraft into it to creating a kind of space tugboat that would gently guide it out of our way to coating part of its surface with a None of these strategies has yet been tested, but NASA has already landed unmanned spacecraft on asteroids, and plans to test a redirection system are under way.

Compared to asteroid impacts, massive volcanic eruptions of

the type that may have triggered mass extinctions in the past are more common and more difficult to anticipate and control. Geologists measure the size of volcanic eruptions on a scale that ranges from M1 (the smallest eruptions) to M9 (the largest). In the last 13.5 million years, there have been at least nineteen eruptions of magnitude M8 or larger, and there is a 75 percent chance of another such eruption happening in the next million years.6 These supervolcanoes—like the one beneath Yellowstone National Park in the United States—are being monitored by geologists, but given that no eruption of magnitude M8 or greater has happened in the modern era—the most recent was twenty-six thousand years ago—we do not really know how to tell the difference between a forthcoming small eruption and one that could spell disaster for life on Earth.

Nor would there be much we could do to prevent the erup-

tion of a supervolcano or mitigate its impact. Aside from the rivers of molten rock and gas hundreds of feet high that would cover everything for hundreds of miles in all directions, the gas and ash

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reflective substance that would cause sunlight to alter its course.5

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have been proposed for protecting us from the impact of any aster-

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it will hit Earth, but if it did, the impact would create a crater more

pouring out into the atmosphere would have global effects that could last for years. The eruption of Mount Pinatubo in the Philippines in 1991—a mere M6—sent enough aerosol gas into the atmo­­ sphere to reduce the amount of sunlight reaching the Earth’s surface, lowering global temperatures by about half a Celsius degree for two years.7 A supervolcano eruption of M8 or M9 could send enough gas into the atmosphere to block enough sunlight that photosynthesis becomes impossible, triggering the death of plants and the animals that depend on them—including humans.

Aside from natural disasters, there are ways in which we could

trigger our own extinction, such as through a catastrophic nuclear war. Less directly, our own activities could cause enough environmental harm that we threaten our own existence. Climate change is expected to negatively impact agriculture and may increase the prevalence of infectious diseases. Climate change also threatens the existence of many other species, particularly those that can live only within narrow climate regimes, and losing them can indirectly impact humans.8 As our population continues to grow and as economic development proceeds, particularly in less developed regions, the impact of our species on the natural world is likely only to grow.

Biologists are concerned that a sixth mass extinction is already

under way because of the number of species that have gone extinct

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in recent centuries and those that are currently threatened with extinction.9 Some species, such as passenger pigeons and Tasmanian tigers, we targeted directly. But many others have disappeared or become threatened because of loss of habitat or competition with invasive species spread around the world by people. As ecosystems lose diversity, they become unstable and prone to further decline.

it is unclear if we will be able to change direction. ■

vival, our species doesn’t have the best track record. A chilling example can be seen deep inside a cave in the Central American country of cher, the cave has become a tourist attraction as a result of both its natural beauty and the amazing archeological artifacts found inside. It takes about half an hour of swimming and wading through an underground river, climbing over boulders, and squeezing through tight passages before you spot the first Maya artifacts. As you climb up from the river, the cave opens up into a large chamber where the shadows of stalactites dance in the light of your headlamp. Fragments of broken pots are everywhere, but it is the human remains that are the most tangible evidence of how desperate people can become when their civilization is on the verge of collapse.

Climbing a makeshift ladder onto a ledge and then ducking

beneath a massive boulder, you reach the spot that gives the cave its name. There lies the skeleton that has become known as the crystal maiden because of the mineral deposits that accumulated on its bones. The crystal maiden and the thirteen other skeletons found deep inside the cave are thought to date to the ninth century AD, a time when the Maya civilization was beginning to unravel.10 The ancient Maya considered caves to be sacred places, home to powerful deities like Chaac, thought to control the rain. Archaeologist Holley Moyes, who was part of a detailed survey of the cave in the 1990s,

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Belize. Known as Actun Tunichil Muknal, or Cave of the Crystal Sepul-

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When it comes to acting in ways that ensure our own long-term sur-

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Our momentum is carrying us toward the sixth mass extinction, and

suspects that the remains found in caves such as those at Actun Tunichil Muknal may have been the result of sacrifices made in a desperate attempt to alleviate drought conditions by appeasing the rain deities.11 Excavations at nearby archeological sites such as Tikal revealed that the drought caused population crashes as drinking water became scarce and crops failed. The Maya people would live on, but their advanced civilization—which had developed sophisticated architecture, art, written language, and mathematics—came to a dramatic end by AD 1000, and the jungle reclaimed their cities.

According to biologist Jared Diamond, the decline of the an-

cient Maya is one of several examples of how human societies can fail as a consequence of the ways in which they interact with their environments.12 Archeological research suggests that by the ninth century, the Mayan population had grown unsustainably large—as many as 14 million people may have been living in the Petén region of Guatemala at the center of the Mayan world. As the population grew, they cleared more and more of the surrounding forest to make room to grow crops like corn and beans. Deforestation and soil erosion reduced the agricultural yield, limiting the amount of food that could be produced. When the droughts began and crops started to fail, people became desperate for resources, and fighting among neighbors increased, which contributed to the population decline.

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Human sacrifices, such as the crystal maiden, seem to have been a last-ditch effort to try to save their civilization.

Diamond sees common threads linking the demise of the Maya

and the collapse of other ancient societies around the world—for example, those of Easter Island, the Anasazi of the southwestern United States, and the Norse of Greenland. Comparing these failures to examples of successful civilizations, Diamond has argued that the

vironment. Deforestation, which contributed to the Mayan collapse, along with overhunting, overfishing, soil degradation, and poor as contributing to the collapse of these once-prosperous societies, factors that continue to threaten modern civilizations. Ultimately, Diamond links all of these environmental problems to a single root billion and growing, we seem to be heading into dangerous territory.

Yet, looking at the factors that affect how vulnerable other

species are to extinction, we may have some cause for optimism.13 On the one hand, larger animals that are high on the food chain and reproduce slowly, all of which are true of humans, are generally at greater risk of extinction. But those with large population sizes and wide geographical ranges are at lower risk, and in those categories we are unrivaled. That there are people living on nearly every speck of land on the planet may increase the chances that at least some will survive any catastrophic natural disaster.

Genetic diversity is another important factor determining ex-

tinction risk, with less diverse species at greater risk because they are both less able to adapt to environmental changes through natural selection and also more vulnerable to the spread of a specialized parasite. As we have seen, our species is relatively low in genetic diversity compared with our closest relatives, but that is changing quickly. What’s more, our ability to rapidly adjust to local conditions through cultural and technological means gives us an edge that no other species possesses. Indeed, species that are able to use a wide variety of different resources, including different types of foods, are generally less prone to extinction, suggesting that we might just

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cause—overpopulation. In that sense, with a global population of 7

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water management are among a dozen factors that Diamond cites

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primary difference is the way that each society interacted with its en-

have a chance. As science writer Annalee Newitz succinctly put it, the keys for humans to survive a mass extinction event will be to “scatter, adapt, and remember.”14

If we do manage to avoid total devastation by an asteroid,

supervolcano, or our own destructive behavior, what will become of our species? Some species still alive today look remarkably similar to ancient fossils, suggesting that long-term evolutionary stasis might be a possibility. The most widely celebrated example came from a discovery made in 1938 in the South African port city of East London.15 Visiting fishermen friends at the docks one morning in late December, Marjorie Courtenay-Latimer, the curator of a local natural history museum, noticed an unusual-looking fish among the daily haul. It was a beautiful shade of blue, with iridescent markings, and had oddly shaped fins. Intrigued, she brought it back to the museum, drew a rough sketch of it, and preserved the skin and bones. She sent the sketch to local fish expert J. L. B. Smith, who just from the drawing recognized it as a coelacanth, a fish heretofore known only from ancient fossils. He was ecstatic—it was like finding a living ­Tyrannosaurus.

The coelacanth was hailed as a living fossil, virtually unchanged

in form from its 80-million-year-old ancestors. Here was a case in which evolution seemed to have been put on hold, suggesting that

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at least some species could persist almost indefinitely just as they are. However, neither the coelacanth discovered by ­Courtenay-Latimer, which was named Latimeria chalumnae in her honor, nor a second kind of living coelacanth later discovered in Indonesia is classified as the same species as those known from the fossil record. The two living species are considered similar enough to be grouped in the same genus, but all known fossil coelacanths are different enough—like

genera. Combining living and extinct species, some ten different genera of coelacanths are known. Although it is true that they share the same way as the limbs of four-legged vertebrates, there are still enough obvious physical differences to classify them in different groups.16 The upshot is that even the best example of an animal that

has changed little over millions of years still evolved into multiple distinct species. What’s more, the physical changes preserved in the fossil record reflect only some of the ways that species can change. An analysis of the genome of Latimeria chalumnae published in 2013 revealed that its genes seem to have been evolving at a slower rate than those of other living vertebrates, supporting the notion that it has indeed evolved, just more slowly than its relatives.17 Although the reasons for its slow rate of change are unknown, the point is that all species evolve. Other so-called living fossils, such as sharks, alligators, and horseshoe crabs, show similar patterns—superficially, modern species resemble ancient forms, but they are not the exact same species. Rather, they beat the odds and avoided extinction, eventually evolving into new forms through a process known as speciation.

What would it take for a new species of human to evolve?

Biologists like to argue about the best way to define “species,” but the definition suggested by Ernst Mayr—that species should be defined by their ability to reproduce with other members of the same ­species—remains among the most widely used by biologists. This is why we consider all dogs to be members of the same species, Canis familiaris, because, although dog breeds can appear noticeably different, most can mate and produce puppies. If species are defined

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many similarities, like their lobe-shaped fins, which move in much

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chimpanzees and gorillas—to be classified as species in different

by their ability to interbreed, then speciation must involve preventing reproduction, and there are several ways that this process can ­happen.

Amazingly, we now know that microbes can play a role in this

process. Chapter 5 detailed how the microbes that live in and on our bodies can play important roles in our biology and that we may have evolved in lockstep with some microbial species. Indeed, we are beginning to understand that at least in some cases, microbes are at least partly responsible for the formation of new species.

For example, fruit flies raised on different diets, such as the

sugars sucrose or maltose, tend to prefer to mate with other flies that were raised on the same diet. A team of Israeli biologists discovered that the mating preference results from differences in the gut microbiomes of flies fed different diets.18 The researchers demonstrated in a laboratory experiment that flies raised on different diets and then treated with antibiotics that kill the gut bacteria lose their preference for same-diet mates. To really prove the point that the microbes were responsible for the preference, they then reinfected the flies with their original gut microbes, and the preferences for same-diet mates were restored. Populations that mate only among themselves will eventually accumulate enough genetic differences through mutations and genetic drift for them to become distinct

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species.

Even more direct evidence that microbes can drive speciation

came from Seth Bordenstein’s lab at Vanderbilt University in Nashville, Tennessee. Bordenstein and his graduate student Rob Brucker discovered that closely related wasp species in the genus Nasonia harbor different communities of gut bacteria and, much like Howard Ochman’s results with humans and great apes, the more closely re-

bial communities.19 What’s more, the gut microbes seem to be keeping species separate. When Bordenstein and Brucker mated males some interspecies pairings produced viable offspring but ­others— for example, N. vitripennis and N. giraulti—did not. If, however, these wasps were reared under sterile conditions that kept their guts soon as the microbes were reintroduced to the wasps’ guts, the offspring were again rendered dead, suggesting that the gut microbes were crucial for maintaining species barriers.

We do not yet know how common it is for microbes to play

a role in speciation by keeping populations reproductively isolated, and we are just beginning to learn not only what microbes are present in the human microbiome but also the many roles they play. What we do know about speciation is that the most straightforward way to prevent reproduction is for populations to be physically separated, such as by mountains or large bodies of water. As such, islands—especially archipelagos (such as the Hawaiian Islands and the Galápagos) are ideally suited for making new species.

The Galápagos finches that helped inspire Charles Darwin’s

discovery of natural selection are a perfect example. Today, there are fourteen species that live on the various islands of the Galápagos, and one on nearby Cocos Island.20 When I was an undergraduate student, my research advisor, Martin Wikelski, asked me to accompany him on an expedition to Galápagos to help with a project on marine iguanas. We camped on tiny Santa Fe, an uninhabited island near the middle of the archipelago. The finches were everywhere and, like all Galápagos animals, the historical lack of predators has made them

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­microbe-free, they had no problem producing healthy offspring. As

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from one wasp species with females from another, they learned that

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lated the wasp species were, the more similar were their gut micro-

fearless. The little finches would land on my head or shoulder, and they tried their best to eat our snacks. I noticed, as Darwin once did, how much variation there was in the beak shape of different finches. This, it turns out, is one of the major differences between species and one of the keys to their evolutionary history.

All of the Galápagos finches are descendants of a single spe-

cies that arrived on the islands from mainland South America about 1 million years ago. Separation from the mainland allowed the founding population to adapt to the local conditions through natural selection, and populations on some islands developed beaks and behaviors that allowed them to specialize on particular types of food—big beaks are helpful for breaking open tough seeds, but long, thin beaks are good for extracting insects from inside a cactus. The distance between islands was enough to allow each population to evolve in relative isolation, the differences between them accumulating until they eventually became different enough to be considered separate species.21

Several years later, as a graduate student, I found myself con-

ducting fieldwork on remote Cocos Island, located about 485 miles northeast of the Galápagos archipelago and home to the only finch in the group outside of the Galápagos. The Cocos finches—which also liked my snacks—all looked more or less identical, having

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­medium-sized beaks that could be used for eating a wide range of different types of food. Unlike the Galápagos archipelago, which had opportunities for finches to evolve in isolation from one another on different islands, Cocos is just one large island. The Cocos finches evolved to be different from their cousins in Galápagos, but on Cocos there were no ways for the finches to diverge any further. The key to speciation is the prevention of sex between populations that

through gene flow with the members of the species they split from. Indeed, genome data suggest that this has happened at least once today.22

If population separation is the easiest way for new species to

form, then just how much isolation would be necessary to result in that many populations have been isolated for hundreds or even thousands of years without undergoing speciation. Native Americans, thought to have migrated to the New World more than fifteen thousand years ago from northeast Asia, would seem to have been among the longest-isolated human populations. But genomic analyses by David Reich, Nick Patterson, and colleagues that compared modern Native Americans to other populations found genetic evidence for at least two different waves of migration from Asia to the Americas, suggesting that gene flow may have persisted over a longer period of time than previously thought.23 Native Americans nevertheless constitute a genetically distinct population because of the combined effects of natural selection during their prolonged isolation and genetic drift following the series of population bottle­necks during their migration. But they never became a distinct s­ pecies.

Since we have no examples of our own species undergoing

speciation, to understand how isolation may contribute to the process in our lineage, we must look at our close relatives. To see the evidence for myself, I paid a visit to paleoanthropologist Rick Potts in his office at the Smithsonian’s National Museum of Natural History. Although I had seen the fossils on display in the Hall of Human Origins, Potts offered to show me some of the specimens in the col-

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speciation in humans? Looking once again at our history, we know

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in Galápagos finches and the same process may be happening again

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are undergoing the process, as incipient species can be reabsorbed

lection that are not on public display. I had worked at the museum as a visiting researcher in the entomology department after finishing my doctoral work, so going behind the scenes into the area off limits to the public was something I had experienced many times. Even so, every time I walked through those brass-framed double glass doors into the restricted area, I still got the same giddy feeling I had the very first time I did it. I will never forget visiting the museum as a child and dreaming about someday working there. It was literally a childhood dream come true.

The museum’s restricted research area is enormous and some-

thing of a labyrinth, and even as a researcher I used to get lost there on a regular basis. Nevertheless, I managed to find my way to the anthropology collections, where cabinets lining the hallway from floor to ceiling were filled with drawers containing human bones. At the end of the hall, I found Potts’s office. He showed me a replica of a fossil skull and bones that were noticeably smaller than most of the others. Potts explained that this specimen, known as the Hobbit for its small size, represents perhaps the best example that we know of in which isolation led to speciation of a close human relative.

The Hobbit skeleton was discovered in a cave on the Indone-

sian island of Flores in 2003.24 Its small size—the skeleton is that of an adult who stood about three feet high and whose brain was

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only about a third the size of modern humans’—stunned the paleo­ anthropology community. Skeptics argued that it must be a diseased Homo sapiens, but the remains of at least nine individuals were discovered, all of them about the same size, and subsequent analyses convinced most of the doubters that the fossils represent a new species of human, dubbed Homo floresiensis. Holding up the replicas, Potts pointed out some of the characteristic physical features of the

the shape of the jaw, all of which resemble primitive species like Homo erectus or the even older Australopithecus. But the Hobbit remains lived as little as eighteen thousand years ago) to be from such old species. Moreover, other features, such as the pelvis, teeth, and shape of the face, were substantially different from those of older species. plained, is that Homo floresiensis evolved from a population of Homo erectus that had made its way to Flores and become isolated, eventually resulting in speciation.

Getting to Flores would not have been a straightforward pro-

cess. The island is located about midway between Australia and the island of Java, where Eugène Dubois discovered the first Homo erectus fossils in 1890. Alfred Russel Wallace, the codiscoverer of natural selection, visited Flores during the years he spent collecting specimens in the region. Based on his observations of what lived where, he noted that Flores and the other nearby islands were home to very different animals than could be found farther west on Java and the islands closest to it. It was odd—the islands themselves seemed quite similar in terms of climate and vegetation and were all roughly the same distance apart, so there were no obvious barriers that would have prevented animals from moving between some but not others. In fact, two of the islands—Bali and Lombok—are separated by fewer than twenty miles but had very different birds and mammals. The turnover in fauna was so dramatic Wallace was able to draw a line on a map that separated the region—to the west of the line, the animals were mostly of the type found in Asia; to the east, they were more typical of Australia and New Guinea.25

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The most likely scenario based on the available evidence, Potts ex-

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were far too recent (initial estimates suggested the species may have

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species, such as the brow ridge on the skull, the bones of the wrist, and



Wallace’s line was later found to follow the edge of the conti-

nental shelf. What Wallace could not see was that the water east of Bali was very deep—deep enough to have kept the islands separate even when sea levels dropped—but to the west it was shallower, and when sea levels were lower, land bridges connected Bali to Java and so on, linking the islands west of the line to mainland Asia.26 So the animals on Java and Bali could have walked, hopped, or flown there without ever having to cross the sea. But to make it to Lombok—and on to Flores—would have meant crossing several stretches of open water, not something Homo erectus was thought to have been capable of doing. Somehow, though, the ancestors of the Hobbits must have made it beyond the horizon, across Wallace’s line to islands filled with strange creatures, from which they would not return.

Potts explained that the current archeological evidence sug-

gests the physical separation that led to speciation in the case of the Hobbits lasted for hundreds of thousands of years. As we have seen, the current trend in humans is exactly the opposite—­populations are more interconnected today than at any point in our history. It would take a significant change to this pattern, such as a major population decline or a complete and prolonged breakdown of our global transportation network, to keep modern people separated from one another. That is, as long as our species is restricted to living

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on Earth.

Although the idea of establishing permanent human colonies

on other planets has long been the domain of science fiction, in recent years there have been more serious discussions about making it a reality. Both governmental agencies like NASA and commercial spaceflight operations have indicated their intention to establish a

already in the process of preparing for just such a possibility. ■

jumpsuits topped with fishbowl-like helmets connected by PVC pipes to rectangular packs on their backs emblazoned with large red Nicoletatos and then led me up a set of steps to a cylindrical white structure. Around us in all directions was a desolate landscape of red rock and sand. Sullivan reached out his hand, covered by heavy black gloves, and opened a thick metal door with a round window. The three of us stepped into a small room, and the heavy door closed behind us. Sullivan pressed a button that promptly turned from white to red, and I watched as a dial on the wall slowly moved from the yellow area on the left that read mars ambient to the blue side on the right: hab ambient. A digital readout above the dial showed a number that steadily climbed, finally stopping at 1,000. Sullivan pressed a button on his radio and spoke into his headset. Another thick door opened, and we stepped inside the Hab.

The Mars Desert Research Station is owned and operated by

the Mars Society, a nonprofit organization whose goal is to support the exploration and colonization of Mars. Teams of four to seven people spend weeks at a time engaged in simulations at the station, which is located in a remote part of the desert in Utah. I arrived on the first full day of simulation for Crew 149, whose members were in the midst of their first crisis. It seemed the diesel generator that provides electricity for the Hab, the primary residential and working

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numbers. They introduced themselves as Ken Sullivan and Pamela

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“Welcome to Mars!” The two people who greeted me wore black

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more permanent human presence outside of Earth. Some people are

space at the station, was malfunctioning. Sullivan and Nicoletatos had been sent to investigate the problem. Their short-term solution was to use a rover (actually a truck) to keep the power running, but that didn’t seem to be working either. The crew’s commander, Paul Bakken, a solidly built Minnesotan with a military background and a perpetually calm demeanor, was busy working on a solution. After a few fuses in the rover blew, he informed them by radio that their only choice was to send a team to the nearest town for supplies. To maintain the simulation to the fullest extent possible, they drove their rover into the tiny town of Hanksville in their spacesuits, helmets and all.

In the meantime, the rest of the crew members were going

about their daily business. Nicoletatos, the crew’s greenhab officer (in charge of the greenhouse where the crew’s plant-based diet is grown) and also its geologist, showed me an experiment the team was running to determine whether sorghum and hops—the raw materials for brewing beer—would grow in soil that is chemically identical to that on Mars. The crew’s biologists, Ann-Sofie Schreurs and Takeshi Naganuma, had begun scouting the area around the Hab for lichens, crusty-looking organisms that consist of a fungus in a symbiotic relationship with an alga. Naganuma, a Japanese biologist whose work on life in extreme environments has taken him to

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places like Antarctica and the bottom of the sea, thought the hardy algal partner of the lichen might be capable of growing on Mars.

Kellie Gerardi, the team’s public affairs officer who works in the

commercial spaceflight industry, showed me some of the crew’s other projects. She pointed out a portable 3D printer the team planned to use to manufacture tools. Her colleagues had already e-mailed her a design for a tool the team hadn’t expected to need—a mousetrap. She

and sleeping quarters were located. The crew’s health officer, Elena Miscodan, a Romanian trauma surgeon, was seated at the kitchen kitchen counter behind her was a box, out of which Gerardi pulled a variety of packages, including salted zebra tarantulas and cricket flour—sources of protein the crew planned to try during their simmal protein than chickens or cattle, making them better candidates for Martian livestock.

Over a lunch of standard Earth-style macaroni and cheese, the

team discussed some of the obstacles that would have to be overcome for colonists to survive on Mars. Ann-Sofie Schreurs, a Belgian biochemist who works for NASA to study the biological effects of radiation and microgravity on the human body, pointed out that both of these would be problems for people living on Mars. Mars has one-third the gravity of Earth, making it less extreme than, say, the moon. But microgravity and radiation both lead to bone loss, at a rate of about 1 to 2 percent bone density lost per month in space.27 This could make it impossible for people who had spent a long time on Mars to return to Earth, because entering the Earth’s atmosphere exposes astronauts to nearly eight times the force of gravity experienced on the surface of the Earth—a person with a weakened skeleton could literally be crushed.

Radiation is an especially big problem for life on Mars. With-

out a magnetosphere or atmosphere to protect the planet, radiation in the form of high-energy cosmic rays, intense ultraviolet radiation, and solar particles hit the surface of Mars at nearly full strength.28 Even the journey from Earth to Mars, estimated to take about six

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ulation. Insects, she explained, are a more sustainable source of ani-

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table checking the contents of a rather large first-aid kit. On the

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led me up a ladder to the upper deck of the Hab, where the kitchen

months, would expose colonists to a dose of radiation equivalent to sixteen times the maximum annual amount allowed by the U.S. Department of Energy for people working with radiation. They would be exposed to a similar amount every five hundred days spent on the Martian surface. Radiation poisoning would be a serious concern for Mars colonists, and spacesuits would not provide much protection, so living quarters will likely have to be built underground. Still, some time will need to be spent on the surface to grow crops (which would also be subject to damaging radiation) and perform other tasks, so some radiation exposure seems inevitable. In addition to bone loss, ionizing radiation damages DNA, directly causing mutations that can lead to the formation of malignant tumors. Preventing cancer would therefore be a much greater difficulty on Mars than it is on Earth.

Despite the challenges, there are many who see colonizing

Mars as a high priority for the near future. In 2014, the commercial spaceflight company SpaceX began construction on a launch facility in south Texas. At the groundbreaking ceremony, its CEO, Elon Musk, said that the first human to visit another planet might depart from that very site.29 Musk is one of many who see permanent human settlements on Mars and other planets as necessary for the long-term survival of our species. As we have seen, asteroid impacts, supervol-

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canoes, and our own destructive behavior may limit the amount of time we can survive on Earth. Mars is the closest planet that offers the possibility of establishing a self-sustainable colony. It has frozen water in the soil in its polar regions and possibly elsewhere, which could be used for human consumption and for irrigating crops. It also has carbon dioxide that could be converted into oxygen, meaning the colonists could produce air they could breathe inside the colony.

mined.

Getting people and supplies to Mars would be one accom-

eral unmanned spacecraft have already made the trip, but none have been designed to return. In part, the difficulty lies in sending enough fuel for a spacecraft to be able to escape Mars’ gravity and engineer Robert Zubrin in 1996, was to avoid the problem of a return trip altogether. In 2011, Dutch entrepreneur Bas Lansdorp established the nonprofit organization Mars One to follow through on Zubrin’s vision. Mars One’s stated goal is to establish a human colony on the Red Planet beginning in 2027, sending colonists there on a one-way trip. Despite the certainty that they would never return to Earth, more than four thousand people applied to be among the first colonists.30 Among them were six of the seven members of Mars Desert Research Station Crew 149.

Sullivan, who has four children ranging in age from fifteen

years to younger than one, discussed the emotional challenge that would come with leaving his family behind if he were to be selected as a Mars colonist. A mechanic who flies an air medevac helicopter for a living and has worked as a military contractor in Iraq, he has faced risks before. But knowingly leaving your children to live on another planet, he said, would be an altogether different endeavor. Nevertheless, Sullivan explained, for him the opportunity to participate in such an epic adventure—one that in his opinion is critical for the continued existence of our species—would justify the personal sacrifice. Still, he said, he hopes his children will be fully grown before he is faced with the reality of actually leaving Earth for good.

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propel it all the way back to Earth. One solution, first proposed by

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plishment—getting those same people back to Earth another. Sev-

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Other materials, such as metals necessary for construction, could be



Establishing a permanent, self-sustained human colony on

Mars would involve people not only living and dying there, but also being born there. To date there has been very little research on reproduction and development in conditions similar to those experienced in space or on another planet. The lower gravity on Mars is especially likely to pose problems for pregnancy, childbirth, and growth. Although studies on fish, amphibians, and birds have suggested that fertilization rates in microgravity are similar to those on Earth, a study by Japanese researchers on embryonic development in mice suggested that mammals might experience more problems than other species.31 When Sayaka Wakayama and colleagues performed in vitro fertilization and grew the resultant mouse embryos in simulated microgravity, they discovered that fewer healthy pups were born than using the same techniques under normal gravity ­conditions.

Also unknown is the impact of being born into an environ-

ment devoid of microbes. Children, as we saw in chapter 5, acquire some of the bacteria their bodies need from their mothers during vaginal births, but pick up others from their surrounding environment. As far as we know, Mars is devoid of microbial life, so the only bacteria that Martian children would be exposed to would be those that were brought—intentionally or unintentionally—from Earth.

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Importing microbes would be necessary not only for human health but also to carry out so-called ecosystem services such as decomposition (imagine the piles of trash that would accumulate if nothing were biodegradable), nitrogen fixation (to convert nitrogen in the atmosphere into a form that can be used), and fermentation (the sorghum and hops could not be made into beer without the help of yeast).

Looking around the table at the group of volunteers willing to

risk their lives on a one-way expedition to the Red Planet, I wondered if these could be the very people who would become the founders of thousands of years, it could lead to the right conditions for speciation. Like finches in an island archipelago, humans living on different planets in our solar system or beyond could evolve independently by

That process might even occur faster on other planets than on

Earth—because radiation alters DNA, tolerable increases in radiation exposure could increase the rate of mutations in our reproductive organs, introducing genetic variation to the gene pool at a faster rate than on Earth. Humans living on Mars or other planets, as well as any other species we bring with us, might adapt more quickly to the dramatically different physical environment by speeding up the process of natural selection. The small initial number of colonists would also mean that genetic drift and gene surfing would play a role in changing the gene pools on extraterrestrial colonies. Perhaps the longterm future of humanity—if we manage to avoid extinction—will involve diversification from the single Earth-bound species known as Homo sapiens to a family of descendant species occupying worlds we are still in the process of discovering. ■ I wasn’t able to stay on Mars for long. Back home in Houston, my wife was eight months pregnant and ready to give birth at any time. Luckily, I made it home before she went into labor. Thomas was born on a Monday morning in a hospital just down the street from where my mother was born. Although she now lived 350 miles away,

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adapting to local conditions through natural selection.

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a new human species. If a Mars colony were to be self-sustainable for

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my mother came to help look after our other two kids for a few days, and my wife’s mother would come later from even farther away. The doctors gave my wife intravenous antibiotics during labor and delivery, a preventative measure due to a positive test for a type of Streptococcus bacteria several weeks earlier. It was standard practice under the circumstances and may have prevented a serious infection, but I couldn’t help but wonder if it would have any impact on the beneficial microbes my son would be exposed to during birth.

Looking at his little face, it was easy to see how much Thomas

resembled his brother and sister, and yet he was clearly his own unique individual. I knew that he had half of my genes and half of my wife’s, but I wondered exactly how many new mutations were in his genome and whether any might be beneficial. I wondered what his life would be like. How long would he live? Would he have kids of his own? Would he be alive to see the first people colonize another planet? Might he be one of them?

All I knew, holding him for the first time in the hospital room,

was that this is the best of what our species does. It is what we have always done, and what—one way or another—we always will do.

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Here, in my arms, was my link to the future of humanity.

Epilogue The last few decades have offered incredible insights into our evolutionary past. We have examined the complete sequences of more than a thousand human genomes from living people and their associated microorganisms and from the remains of those who preceded us. Combining this information with historical population records and data from large biomedical studies has revealed that natural selection proceeded through the development of agriculture and industry and continues to affect people in modern times. Infectious diseases, including old adversaries such as malaria but also new threats—like Ebola—are especially likely to continue to act as selective agents in our evolutionary future. Yet, we have also seen how other evolutionary forces—mutation, sexual selection, genetic drift, and gene flow—have impacted our species and that they still do so today.

But the changes that have accompanied modernization have

altered the way each of these forces affects our continuing evolution. Our large global population size combined with a trend toward older fathers means that there are more mutations occurring in ba179

bies born today than ever before in our history. Mutations are the ultimate source of genetic variation, so our gene pool has never had a richer source of raw material for natural selection to work with than it does today.

Natural selection is still occurring, but not always in the same

way as it has in the past. An individual’s chances of survival, as well as the number of children he or she will leave behind, is now determined in large part by cultural influences, including socioeconomic status and access to modern health care, medicine, and birth control. There are still major disparities between more developed and less developed regions of the world that affect life expectancy and the influence of infectious disease. Increasingly, though, technology and medicine are weakening the connection between a person’s genes and his or her survival and reproductive success. Although antibiotics and medical procedures such as Cesarean sections save lives, they are nonetheless having unintended harmful effects on microorganisms that have been our long-term evolutionary partners. We do not yet know what losing them will mean for our future.

Demographic changes, especially the declining birth and death

rates that accompany economic development, have also had major effects on the strength, impact, and direction of selection. Such demographic transitions make selection on traits that affect fertility particularly important for our ongoing evolution. We still know comparatively little about how sexual selection has affected our evolutionary history, and what we know about it from the past may not

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be so relevant for the future. The way we choose our sexual partners is changing, and preferences that evolved to assess the genetic quality of potential mates do not necessarily lend themselves to modern matchmaking. At the same time, the widespread use of birth control

means that people have much more control over their own reproduction, further diminishing the importance of our genes. The movement of people around the world is another way in

have no historical precedent. Migration has been important throughout our species history, and populations—and even closely related species—have always exchanged both genes and germs. But the rate at which migration is happening today means that our species is quickly approaching a point at which we are no longer comprised of distinct populations that occasionally swap genes. Rather, we are becoming a single global population with one rapidly swirling gene pool. Any beneficial mutation that arises in one part of the world can quickly spread—but so, too, can new diseases.

I began this book with the observation that many scientists

are reluctant to make predictions about the future of our species. Given all the ways that modernization is affecting our evolution, it is easy to see why extrapolating from the past into the future can be problematic. Yet, as I hope I have shown, there is a lot we can learn about our continuing evolution from looking at the evolutionary forces that affected our ancestors and how those forces are changing. New information is accumulating rapidly, especially in big data fields such as genomics and the study of the microbiome.

There are also potential game-changing developments on the

horizon that could alter our evolutionary trajectory in such ways that the lessons of the past will offer little help in predicting the future. We explored one of these, the colonization of other planets, which could lead to the origin of new species of humans through the evolutionary process of speciation. Although the planets in our

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which modern life is affecting our ongoing evolution in ways that

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and assisted reproductive technology such as in vitro fertilization

solar system do resemble islands in an archipelago, the analogy becomes limited when we consider how fundamentally different the environments are on these other worlds as compared to the planet we have inhabited for the last 4 billion years. Yet those differences might drive natural selection to favor adaptations that make us better suited to what currently seem like hostile environments.

The other future development that could fundamentally alter

our evolutionary course, and for which there is no historical precedent, is the widespread use of human genetic engineering. Gene therapy, in which particular genes are intentionally modified to achieve a desired outcome, has been performed in several nonhuman species and is being explored as treatment options for congenital diseases such as hemophilia or cystic fibrosis. But modifying the genes of adult somatic cells—all cells of the body other than those that produce sperm and eggs—would have an effect only on that particular individual. In 2015, Chinese researchers announced that they had edited genes within human germline cells—those that form sperm and eggs—opening up the possibility that changes made in the lab could be passed on from generation to generation just like a natural mutation.1

Although this technique has the potential to lead to heritable

cures for genetic diseases, it also raises ethical questions about how such technology should be used. In December 2015, an international summit was held in Washington, D.C., to discuss the implications of the new gene-editing technology.2 The result was a recommenda-

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tion that the technology was appropriate for laboratory research but should not be used on human embryos intended to result in a ­pregnancy—at least for now.

Human germline engineering could give us the ability to guide

ment. Science historian Nathaniel Comfort has pointed out that the modern discipline of medical genetics can be traced directly back to ics, which sought to improve the human condition by controlling reproduction. Twenty-first-century genetic engineering is a far cry from the racist ideologies of the Nazis, who distorted eugenic principles to serve their political agenda. But the fundamental pitfalls involved in any attempt to guide human evolution remain. Comfort stated the situation well in his 2012 book, The Science of Human ­Perfection—“Deliberate efforts at human improvement may have the population’s best interests at heart, but willy-nilly they involve social control.”3

Clearly, there are serious ethical considerations that would

come with making heritable changes to the genes of some people and not others. On the other hand, if such technologies are available to just a select few, their influence on our species as a whole would be minimal. But there is also the reality that we are still a long way from understanding what each of our genes actually does, how it interacts with other genes, and how those genes are turned on and off to control their functions in different parts of the body and at different times in human development. Now that we have sequenced the human genome, we may be able to read life’s instruction manual, but that doesn’t mean we understand everything it says.

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the nineteenth- and early twentieth-century philosophy of eugen-

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our own evolution, though this is not necessarily a good develop-

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Notes

I NTRO DU CTI O N   1. Charles R. Darwin, The Descent of Man and Selection in Relation to Sex (London: John Murray, 1871).   2. John Gurche, Shaping Humanity: How Science, Art, and Imagination Help Us Understand Our Origins (New Haven: Yale University Press, 2013).   3. Theodosius Grigorievich Dobzhansky, Mankind Evolving: The Evolution of the Human Species (New Haven: Yale University Press, 1962).   4. Ernst Mayr, Animal Species and Evolution (Cambridge: Belknap, 1963); Stephen Jay Gould, “The Spice of Life: An Interview with Stephen Jay Gould,” Leader to Leader 15 (2000): 14–19; Ben Dowell, “David Attenborough: ‘I Don’t Ever Want to Stop Work,’” Radio Times, September 9, 2013, http://www.radiotimes.com/news/2013-09-09/david -attenborough-i-dont-ever-want-to-stop-work (accessed September 1, 2015).   5. John A. Endler, Natural Selection in the Wild (Princeton: Princeton University Press, 1986).   6. Christopher Wills, Children of Prometheus: The Accelerating Pace of Human Evolution (New York: Basic Books, 1998).   7. Herbert George Wells, The Time Machine (New York: Henry Holt, 1895).   8. Keith M. Johnston, Science Fiction Film: A Critical Introduction (London: Berg, 2013).

1. G E N OM E S

AN D

G E R MS

  1. James Shreeve, The Genome War: How Craig Venter Tried to Capture the Code of Life and Save the World (New York: Ballantine Books, 2007); Tim Radford, “Scientists Fin-

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Seth R. Bordenstein, “Disruption of the Termite Gut Microbiota and Its Prolonged Consequences for Fitness,” Applied and Environmental Microbiology 77 (2011): 4303–12. 36. Sarah C. P. Williams, “Gnotobiotics,” Proceedings of the National Academy of Sciences 111 (2014): 1661; Peter J. Turnbaugh, Ruth E. Ley, Micah Hamady, Claire Fraser-Liggett, Rob Knight, and Jeffrey I. Gordon, “The Human Microbiome Project: Exploring the Microbial Part of Ourselves in a Changing World,” Nature 449 (2007): 804; Ki-Jong Rhee, Periannan Sethupathi, Adam Driks, Dennis K. Lanning, and Katherine L. Knight, “Role of Commensal Bacteria in Development of Gut-Associated Lymphoid Tissues and Preimmune Antibody Repertoire,” Journal of Immunology 172 (2004): 1118–24. 37. Junjie Qin, Ruiqiang Li, Jeroen Raes, Manimozhiyan Arumugam, Kristoffer Solvsten Burgdorf, Chaysavanh Manichanh, Trine Nielsen, et al., “A Human Gut Microbial Gene Catalogue Established by Metagenomic Sequencing,” Nature 464 (2010): 59–65. 38. Ilana Zilber-Rosenberg and Eugene Rosenberg, “Role of Microorganisms in the Evolution of Animals and Plants: The Hologenome Theory of Evolution,” FEMS Microbiology Reviews 32 (2008): 723–35.

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E PI LO G U E 1. Puping Liang, Yanwen Xu, Xiya Zhang, Chenhui Ding, Rui Huang, Zhen Zhang, Jie Lv, et al., “CRISPR/Cas9-Mediated Gene Editing in Human Tripronuclear Zygotes,” Protein & Cell 6 (2015): 363–72. 2. Sara Reardon, “Global Summit Reveals Divergent Views on Human Gene Editing,” Nature 528 (2015): 173. 3. Nathaniel Comfort, The Science of Human Perfection: How Genes Became the Heart of

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American Medicine (New Haven: Yale University Press, 2012).

Acknowledgments Creating this book has been an amazing process, and one that would not have been possible without the kindness, generosity, and support of many people. First, I would like to acknowledge the contributions of the students in Rice University’s Introductory Biology II courses over the last six years, with whom I discussed many of the ideas that are explored in this book. Your curiosity and stimulating questions helped inspire my interest in the ongoing evolution of our species.

A version of part of chapter 3 was published as an article in

Nautilus, where it benefited from the guidance and editing of Michael Segal. Discussions with Joan Strassmann and Rob Dunn encouraged me to take the next step in creating this book by finding a literary agent. I am extremely grateful to Don Fehr and his staff at Trident Media Group for taking me on as a client, for all the support and encouragement along the way, and for being patient with all of my questions about the strange (to me) world of book publishing. Jean Thomson Black was an equally capable guide; Jean, along with Ann-Marie Imbornoni and the rest of the team at Yale University 213

Press, helped balance scholarly detail and palatability for the general public and crafted an original and creative visual design. Robin Du­ Blanc’s masterful copyediting helped keep the narrative flowing and the grammatical gaffes to a minimum. I must also thank the orga­ nizers of the Santa Fe Science Writing Workshop, Sandra Blakeslee and George Johnson, as well as Tim Appenzeller and the other instructors and participants, who helped me develop a toolkit with which I might share my passion for science.

I am extremely grateful to the many individuals who dis-

cussed the details of their work and their lives with me, patiently answering my questions and in many cases inviting me into their offices, labs, field sites, homes, and simulated Martian colonies. They include Robin Baker, Paul Bakken, Cynthia Beall, Martin Blaser, Seth Bordenstein, Gregory Buck, Denise Dearing, Anna Di Rienzo, Maria Gloria Dominguez-Bello, Jennifer Drummond, Alain Gagnon, Kellie Gerardi, Richard Gibbs, David Graham, Henry Harpending, Kristen Hawkes, John Hawks, Ed Hollox, Nina Jablonski, Pan-Pan Jiang, Elinor Karlsson, Damian Labuda, Pierre Lafontaine, Daniel Levy, Cecil Lewis, Dan Lieberman, Francine Mayer, Emmanuel Milot, Claudia Moreau, Holley Moyes, Takeshi Naganuma, Pamela Nicoletatos, Rasmus Nielsen, Howard Ochman, David Perrett, Normand Perron, Rick Potts, Lita Proctor, David Reich, Pardis Sabeti, Stephen Schaffner, Ann-Sofie Schreurs, Stephen Stearns, Ken Sullivan, Randy Thornhill, Sarah Tish-

AC KN OW LE DGMENTS 

214

koff, and Nathan Yozwiak. I am particularly indebted to Emmanuel Milot, Pardis Sabeti, the organizers and participants of the EMBO conference on human evolution in the genomic era, and Mars Desert Research Station Crew 149 for hosting me for extended visits.

I also wish to offer my sincere gratitude to the following indi-

viduals for taking the time to read and provide feedback on partial

Stephen Bradshaw, Kellie Gerardi, Kristen Hawkes, Ed Hollox, Elinor Karlsson, Cecil Lewis, Emmanuel Milot, Holley Moyes, Howard Ochman, Rick Potts, David Reich, Pardis Sabeti, Adrienne Simões-Correa, Catharina Solomon, Stephen Stearns, and Randy Thornhill. A special thanks goes to my friends Jeffrey Lewis, Joan Strassmann, and Kelly notice) and provided extremely helpful comments and ideas; this book was very much improved by your critical insights and thoughtful suggestions. Two anonymous readers provided additional assistance by pointing out inaccuracies and highlighting instances in which additional examples, viewpoints, and explanations were needed to balance the narrative or clarify a concept. Any remaining errors or omissions are my own responsibility.

Stephen Bradshaw, Mike Gustin, Brian Maitner, Susan McIn-

tosh, Stephen Stearns, and the staff of the Framingham Historical Society helped me to identify useful sources and material. Gabriela Zambrano assisted with interview transcription. I am fortunate to have had support from my colleagues at Rice and from two department chairs, Janet Braam and Evan Siemann. Additional thanks is due to the many people who helped keep me calm, cool, and caffeinated through the various stages of research, writing, and editing— especially the staff of Rice Coffeehouse, Café Brasil, and the wonderful students and A-Team at Baker College, my home for the last five years.

My family has always been the foundation upon which my life

is constructed, and I’ve been fortunate to build one filled with joy and love. At its core are my children, Nyala, Nicholas, and Thomas, who never cease to amaze me with their energy, empathy, and unend-

2 15

Weinersmith, who read complete drafts of the entire book (on short

AC KNOW L E D GM ENTS 

drafts: Robin Baker, Cynthia Beall, Martin Blaser, Seth Bordenstein,

ing affection. I am eternally grateful to Ira and Susan Solomon—for pretty much everything, but especially for always encouraging me to pursue my dreams and for making me believe they are attainable. Family trips with my parents and sisters taught me to seek out new ideas and experiences and fostered a love of travel that has fueled a lifetime of exploration. My extended family has given me a network of loving supporters, including my wonderful in-laws. I continue to be inspired by the lives of Bob and Flavia Horth, whose example gives me hope for the future of our species—and not only because they raised four incredible daughters.

The final thanks goes to my wife, Catharina, for always re-

minding me about what is most important in life. Without your patience, love, and support, this book would not exist. Thanks for taking

AC KN OW LE DGMENTS 

216

a chance on the guy in the wrong jacket.

Index

apes and monkeys: ancestors of, 3; brain

ABI 3100, 19–20 acclimatization, 57, 58–59

evolution, 47, 48; genetic diversity of,

acute mountain sickness, 55–57

41–42; microbiomes, 135–36; populations of, 190n6

Africa: brain size studies, 47–48; fossil humans, 5–6; and genetic diversity, 42;

ASPM, 47–48

migration from, 5, 42–43; skin color,

assisted reproductive technology, 121–23

50–53

asteroid impacts, 156–57

age at first reproduction, 68–70, 77, 82–83,

athletes, 57 Attenborough, David, 7

86–87 agriculture, 30, 69–71

Australopithecus afarensis, 5

air travel, 31, 54, 55

averageness, 102, 106, 108, 113

alleles, 25, 26, 28, 62, 63 Allison, Anthony Clifford, 23–26 bacteria, evolution of, 7–8. See also human

Amhara people (Ethiopia), 61

microbiome

amylase gene, 70 Anasazi people, 160–61

Baker, Paul, 57–59

ancient DNA, 64–68, 70, 139, 140–41

Baker, Robin, 116–18, 123–24

Andean high-altitude adaptations, 57–59,

Bakken, Paul, 172

60–61, 62, 63

Bates, Henry Walter, 37, 189n1

animal domestication, 30, 68

Beall, Cynthia, 59–60, 61–62, 63

ant fungus gardens, 128–30

Bellis, Mark, 117–18

antibiotic resistance, 7, 32

big data, 37–72; and dietary adaptation studies, 68–71; and genetic diversity

antibiotics, 130, 143–48, 180

217

big data (continued)

Chinese people and amylase gene, 70

studies, 40–43; genome sequencing

cholesterol levels, 86

methods and, 39–40; high-altitude

chromosomes, 16, 22, 120–21

adaptations studies, 55–64, 67–68;

chronic mountain sickness, 58

population genetics and genetic drift,

church records, 75–76, 78

55–64, 67–68; skin color evolution

climate change, 158

studies, 49–55

Clinton, Bill, 15

Birkhead, Tim, 118

Clostridium difficile, 147–48

Birney, Ewan, 40

Cocos Island finches, 166–67

birth control. See contraception

coelacanths, 162–63

birthrates, 82–83, 87, 180

Cold Spring Harbor Symposium on Popu-

births. See reproduction and fertility

lation Genetics (1955), 44

Blaser, Martin, 144–47

Collins, Francis, 15

body hair, 49, 192n19

Comfort, Nathaniel, 183

Boisvert, Mireille, 76

contraception, 111–12, 119, 124

Bordenstein, Seth, 164–65

convergent evolution, 53

bottleneck pattern, 43

Cooper, Alan, 140–41

Boulangerie Bouchard, 80–81

coprolite microbial DNA, 141

brain size, 47–49

coral and Symbiodinium, 148–49

breeding value, 77, 79–80

Courtenay-Latimer, Marjorie, 162

Brown, Louise and Natalie, 121, 122–23

culture as agent of evolutionary change,

Brucker, Rob, 164–65 Bryson, Bill, 156

68–70, 86–87, 180 Currie, Cameron, 128

bubonic plague, 30 Byars, Sean, 85, 87–88 Daedalus: or, Science and the Future

I N DEX  

21 8

(Haldane), 123–24 cancer, 32, 49, 50, 53, 144, 145, 146, 174

dairy consumption, 68–70

capillary sequencers, 19–20

Darwin, Charles, 4–5, 38–39, 97, 104

cardiovascular disease, 32, 71, 85, 86, 146

Davies, Julian, 132

Cavalli-Sforza, Luigi Luca, 79

Dawkins, Richard, 10–11

Cave of the Crystal Sepulcher (Belize), 159

death rates, 82–83, 87, 131, 180

Celera genomics, 15–16

demography and demographic transi-

Cesarean sections, 142–43, 146, 148, 149

tions: Framingham Heart Study data

Chaplin, George, 50, 51–52

and, 85–87, 89–92; in Gambia, 83–84;

Children of Prometheus (Wills), 9

on Île aux Coudres, 76–79, 80–83; in

chimpanzees. See apes and monkeys

nineteenth-century Utah, 83; use of

Eskimo-Aleut people, 52

78–79

Ethiopian high-altitude adaptations, 61,

Denisovans, 66–67, 67–68

62, 63 eugenics, 6–7, 102, 183

Descent of Man and Selection in Relation

eumelanin, 50, 51

to Sex, The (Darwin), 4–5, 97, 104 Di Rienzo, Anna, 61, 63–64, 68 diabetes, 32, 71, 146, 148 Diamond, Jared, 160–61 dietary adjustments, 68–71 DNA: genetic drift and, 45; genome

Europeans: brain size studies, 47–48; lactose intolerance, 69–70; origins, 65; skin color, 52–53 evolution, agents of, 9, 68. See also culture; gene flow; genetic drift; mutations; natural selection

sequencing, 15–20, 40–41; microbial,

evolutionary biology, 44

135–36, 139–41; natural selection and

evolutionary psychology, 100–101

changes in, 48, 50, 52; radiation and, 174,

Ewbank, Doug, 85, 87–88

177; repair mechanisms, 120; studying

extinction, 155–62; asteroid impacts and,

ancient, 64–68, 70, 139, 140–41; swap-

156–57; loss of genetic diversity and,

ping, 22–23

161–62; overpopulation and, 159–60;

Dobzhansky, Theodosius, 7, 9

volcanic eruptions and, 157–58

Domagk, Gerhard, 143 Dominguez-Bello, Maria Gloria, 137, 146 Dubois, Eugène, 5, 169

facial perception and preferences, 100–106

dung flies, 116

feces transplants, 147–48

Durban, Richard, 42

feminine/masculine faces, 103, 108 fertility. See reproduction and fertility Fisher, Ronald, 44

East Asian skin color, 52–53

Fleming, Alexander, 143

Ebert, Dieter, 91

Flores (Indonesia), 168–70

Ebola virus, 21, 28–29, 31

folate deficiency, 50–51

economic development, 79–80, 82, 93,

fossil humans, 3–6, 66, 162–63, 167–70

155, 180. See also industrialization;

FOXP2, 48–49

modernization

Framingham Heart Study, 85–87, 89–92

ectogenesis, 123–24

fruit flies, 84, 121, 164

education and reproduction, 82, 88

fungi (fungus), 7–8, 127, 128–30

EGLN1, 62 Endler, John, 8 EPAS1, 62, 67–68

Galápagos finches, 165–66

Escovopsis spp., 128–30

Galton, Francis, 6–7, 102

2 19

dental remains, 140–41

I N DEX  

church records in study of, 75–76,

Gambia, demographic transition in, 83–84

height and mate choice, 106–7, 108, 110, 115 Helicobacter pylori, 144–47

Gangestad, Steven, 105, 108–9

hemoglobin, 58–59

gene flow, 55, 64–67, 68, 71, 166, 167

heterozygotes, 25, 186n10

gene surfing, 46, 177

high-altitude environment adaptations,

generation times, 32

55–68; acute mountain sickness, 55–57;

genetic diversity, 40–43, 161

in Andeans, 57–59, 60–61, 62, 63; in Den-

genetic drift, 45–48, 71–72, 164, 167, 177

isovans, 67–68; in Ethiopians, 61, 62, 63;

genetic engineering, 182–83

genetic basis of, 61–64; in Sherpa people,

Genographic Project, 40–41

63; in Tibetans, 59–60, 60–61, 62–64, 68

genome sequencing, 15–20, 40–41

histocompatibility, 108–9

genomes, 16–17

HIV/AIDS, 7–8, 31, 32

Gerardi, Kellie, 172, 173

Hobbit skeleton, 167–70

germline engineering, 182–83

holobionts, 150

Gomendio, Montserrat, 119

hologenome theory, 150

Gould, Stephen J., 7

hominins, 5. See also fossil humans

Govindaraju, Diddahally (Raju), 84–85,

Homo erectus, 5, 169, 170

87–88 Graham, David, 147

Homo floresiensis (Hobbit), 168–70 Homo sapiens: age of, 5; debate on con-

Grammer, Karl, 104

tinuing evolution of, 6–9; evolutionary

grandmothers, 89–92

future of, 9–12; extinction, 155–62;

great apes. See apes and monkeys

fossil records of early evolution of, 3–6, 66, 162–63, 167–70; genetic diversity of, 40–43; germline engineering and,

H1N1, 31

182–83; long-term evolutionary stasis

Hadfield, Jarrod, 79–80

and, 162–63; migration, 42–43, 54;

Hadza (Tanzania), 89–90

possible evolution of new species of

I N DEX  

220

hair, 49, 192n19

(see speciation)

Haldane, J. B. S., 44, 123–24, 186n10

Human Genome Project, 15–16

Hancock, Jeffrey, 114–15

human microbiome, 127–51; antibiotics

hand sanitizers, 130

and, 143–48; attempts to eliminate

handicap principle, 98–99

microbes, 130–31; differences between

HapMap Project, 40–41, 42, 63

traditional and urban industrial life-

Harcourt, Alexander, 119

styles, 137–39; feces transplants and,

Harvard Medical School, 64–65

147–48; helpful, harmful, along for the

Hawkes, Kristen, 89–90, 91

ride, 127, 148; hologenome theory and,

health care, 77, 82, 83, 91, 180

150; implications of losing microbial

influenza, 30, 31

134–35; lessons from other species,

Internet dating, 112–15

128–30, 148–49; and Mars colonization,

interplanetary travel and colonization, 170–77

ean sections, 142–43; microbes as coev-

interracial marriages, 55

olutionary partners, 131, 135–36, 149–50,

interspecies gene flow, 66–68

164; of modern vs. ancient people, 139–42;

isolation, 76–79, 80–83, 165–70

National Institutes of Health Research and Human Microbiome Project, 131–34; probiotics and, 147; rapidly evolving

Jablonski, Nina, 49, 50, 51–52

microbes and adaptability, 150–51; and

Japanese people and amylase gene, 70

sanitation, 130, 141–44; uniqueness of,

Jokela, Markus, 110

135–37; use of term, 204n7 Human Microbiome Project, 133 Human Sperm Competition (Baker and Bellis), 117

kamikaze sperm, 118 Kenya, sickle cell and malaria, 23–24

Hurtado, Alberto, 58

keratinocytes, 50

Huxley, Julian, 203n41

Khan, Sheik Umar, 28, 29 Kim, Peter, 90 Kimura, Motoo, 43–46

Iceland, age of fathers and mutations in, 92–93 Île aux Coudres, 76–79, 80–83

lactose intolerance, 68–70

immigration. See migration

language, 48–49

immune system, 108–9, 145, 148

Lansdorp, Bas, 175

in vitro fertilization, 121–23

LARGE, 27–28

industrialization, 53, 82, 93, 106, 138,

Lassa hemorrhagic fever, 27–28

142. See also economic development;

Latimeria chalumnae, 162–63

modernization

LCT, 69–70

infectious diseases and evolution, 20–33;

leafcutter ant symbiosis, 128–30

agriculture and zoonotic diseases,

Lederberg, Joshua, 132

29–31; development of agriculture and,

Leicester conference (April 2014), 39, 40,

30; emerging diseases, 31–33; Lassa

41, 42, 61–62

hemorrhagic fever, 27–28; malaria,

Lewis, Cecil, 138–39, 140, 141

22–27; Sabeti’s research on, 20–23;

Lieberman, Dan, 192n19

testosterone on, 108

life expectancy, 180

infertility. See reproduction and fertility

life history, 76, 84

2 2 1

176; maternal acquisition of, and Cesar-

I N DEX  

partners, 148–51; individual differences,

living fossils, 162–63

microcephaly, 47–48

long-range haplotype test, 23

microgravity, 173, 175

Lucy (fossil skeleton), 5

migration, 5, 42–43, 54–55, 181

Lummaa, Virpi, 79

milk, 68–70 Milot, Emmanuel, 75–82 Miscodan, Elena, 172–73

malaria, 22–27, 30, 111–12, 186n10

Missing Microbes (Blaser), 146

male competition, 115–19

MIT Center for Genome Research (White-

Mankind Evolving (Dobzhansky), 7 Marques-Bonet, Tomas, 41 Mars Desert Research Station, 171–73 Mars exploration and colonization, 171–77

head Institute), 20 modernization, 110–11, 124, 148, 179–81. See also economic development; industrialization

Mars One, 175

mole voles, 121

Marshall, Barry, 145

Monge, Carlos, 58

masculine/feminine faces, 103, 108

monkeys. See apes and monkeys

mate choice, 100–115; attractiveness

Moorad, Jacob, 83

and fertility, 109–11; biological reasons

mosquito fish, 84, 87

for preferences, 107–8; birth control

mother hypothesis, 89

pills and, 111–12; and evolutionary

Mount Pinatubo eruption, 158

psychology, 100–101; facial perception

mountain sickness, 55–57, 58

and preferences, 100–106, 108; height

Moyes, Holley, 159–60

and, 106–7, 110; and histocompatibility,

MRSA (methicillin-resistant Staphylococ-

108–9; odor and, 105–6, 108–9, 110–11;

cus aureus), 32

online dating and, 112–15; peacock tail

Mueller, Ulrich, 128

feathers and, 97–98

Musk, Elon, 174

Mayan collapse, 159–60

mutations: father’s age and, 91; frequency

Mayer, Francine, 76, 78, 80, 82

of, 64; and future humans, 179–80; as

Mayr, Ernst, 7, 163

harmful, 17, 25; in mammals, 45; popu-

McGregor, Ian, 83–84

lation size and, 41, 71–72; radiation and,

melanin, 49–53

174, 177

melanocytes, 50

I N DEX  

222

menopause, 89–92 microbe-free humans on Mars, 176

Naganuma, Takeshi, 172

microbe-free rabbits and mice, 149

NASA, 156–57, 170

microbial DNA, 135–36, 139–41, 149–50

Nasonia spp., 164–65

microbiome. See human microbiome

National Human Genome Research

microcephalin, 47–48

Institute (NIH), 131–34

131–32, 133 Native Americans, 167

Ötzi the Iceman, 140 oxygen. See high-altitude environment adaptations

and, 4–5, 38–39; and dietary adjustments, 68–71; and genetic diversity, 43; vs. genetic drift, 45–48; high-altitude adaptation (see

Pääbo, Svante, 66, 139

high-altitude environment adaptations);

Panama, túngara frogs, 99

infectious diseases and, 20–33; and recent

Parker, Geoffrey, 116

and ongoing evolution, 7–12; and skin

Patterson, Nick, 65–68, 167

color, 49–55; Wallace and, 37–39. See also

peacocks and sexual selection, 97–98

reproduction and fertility; sexual selection

penicillin, 143

Natural Selection in the Wild (Endler), 8

Perrault, Pierre, 81

Nature, 45

Perrett, David, 101–3, 105, 106, 107

Neanderthals (Homo neanderthalensis),

Peru, high-altitude adaptation in, 56–57,

4, 66, 67

58–59

neural tube defects, 50–51

Pham, Michael, 119

neutral theory of molecular evolution, 45–46

Philippe, Pierre, 76

New Scientist, 118

photographic blending technique, 102

Nicoletatos, Pamela, 171–72

Plasmodium falciparum, 25–26

Nielsen, Rasmus, 67–68

population, increasing, 30, 31, 72, 159–60

nitric oxide, 60

population genetics, 44

nucleotides, 16, 19, 25, 41

Potts, Rick, 167–70

nutrition, 51, 54, 77

pregnancy, 62–63, 120, 176. See also reproduction and fertility Prevotella sp., 139, 141

obesity, 146–47

probiotics, 147

Ochman, Howard, 135–36

Proctor, Lita, 131, 136–37

odor cues, 105–6, 108–9, 110–11 On the Origin of Species by Natural Selection (Darwin), 38–39

radiation and DNA, 173–74, 177

1,000 Genomes, 41, 42

Reich, David, 64–68, 167

online dating, 112–15

reproduction and fertility: age at first

“Only Good Helicobacter pylori is a Dead Helicobacter pylori, The” (Graham), 147 Origin of Species. See On the Origin of Species by Natural Selection (Darwin)

reproduction, 68–70, 77, 82–83, 86–87; and contraception, 119; declines in sperm counts, 119–21; folate and ultraviolet radiation and, 50–51; and high-altitude

2 2 3

natural selection: and culture, 180; Darwin

Oromo people (Ethiopia), 61

I N DEX  

National Institutes of Health (NIH),

reproduction and fertility (continued) adaptation, 62–63; on Île aux Coudres,

Sierra Leone, Ebola virus outbreak, 21, 28–29

76–79, 80–83; in vitro fertilization, 121–23;

single nucleotide polymorphisms, 41, 52

on Mars, 176; menopause and, 89–92;

skin cancer, 50, 53, 192n23

sex as separate from, 123–24; and sexual

skin color, 49–55

selection, 109–10. See also demographic

SLC24A5, 52–53

transitions; sexual selection

Smithsonian’s National Museum of

response to selection, 53, 79–80, 88, 92

Natural History, 4, 5, 6, 167–70

rice domestication, 70

space travel, 170–77

rickets, 51

SpaceX, 174

Roldán, Eduardo, 119

speciation, 163–78; finches and island iso-

Roman Catholic Church, 75, 78–79

lation, 165–67; Homo floresiensis (Hob-

Ryan, Mike, 99

bit) and island isolation, 168–70; and interplanetary travel and colonization, 170–77; microbes as drivers of, 164–65;

Sabeti, Pardis, 20–23, 27–29, 46 Saint Lawrence River community, Île aux Coudres, 76–79, 80–83

Native Americans and isolation, 167 species, definition of, 163–64 sperm competition, 115–19

salivary amylase, 70

sperm counts, 119–21

Sanger’s chain termination method, 18–19

Sperm Wars (Baker), 117

Schreurs, Ann-Sofie, 172, 173

spina bifida, 50

Science, 132

SRGAP2, 48

Science of Human Perfection, The (Com-

Stearns, Steve, 84–89, 87–88, 91

fort), 183

sterilization and sanitation, 130, 141–44

scorpionflies, 104

sulfonamide, 143

self-domestication hypothesis, 91

Sullivan, Ken, 171–72, 175

sex and reproduction, separation of, 123–24

sunlight, 49–55, 149–50, 158, 192n24

Sex in the Future (Baker), 123–24

sunscreens, 49–50, 53, 54

sexual selection, 97–100; and the

Symbiodinium and coral, 148–49

handicap principle, 98–99; infertility

symbiosis, 128–30, 148–50

and, 119–24; male competition and (see

symmetry, 103–6

male competition); mate choice (see mate choice); separation of sex from

I N DEX  

224

reproduction and, 123–24

termites, 149

Shackelford, Todd, 118, 119

Thornhill, Randy, 103–6, 107, 108–9

Sherpa people (Nepal), 63

Tibetan high-altitude adaptations, 59–61,

sickle cell trait, 24–26, 186n10

62–64, 68

Ward, Ryk, 22

Toma, Catalina, 114–15

Warren, Robin, 145

Treponema sp., 138–39, 141

wasps (Nasonia), 164–65

tuberculosis, 30

Wedekind, Claus, 109

túngara frogs (Panama), 99

Wells, H. G., 9 Wikelski, Martin, 165–66 Williams, George, 89

ultraviolet radiation, 49–55, 71, 173–74

Wills, Christopher, 9

University of Texas at Austin, 19–20

Wright, Sewall, 44–45, 46

Utah, demographic transition in, 83 Y chromosome genes, 120–21 Venter, J. Craig, 15 viruses, evolution of, 7–8 vitamin D, 51–52, 53, 54, 192n24

Yanomami people (Venezuela), 137–38, 205n14 Yoruba people (West Africa), 27–28

volcanic eruptions, 157–58 zebra fish, 52 Wakayama, Sayaka, 176

zoonotic diseases, 30–31

Wallace, Alfred Russel, 37–39, 169–70

Zubrin, Robert, 175

2 2 5

wandering albatross, 75–76

Tishkoff, Sarah, 70

I N DEX  

Time Machine, The (Wells), 9