Who We Are and How We Got Here: Ancient DNA and the New Science of the Human Past

by David Reich

I also highlight some of the great themes that are emerging, especially the finding that mixture between highly differentiated populations is a recurrent process in the human past. Today, many people assume that humans can be grouped biologically into “primeval” groups, corresponding to our notion of “races,” whose origins are populations that separated tens of thousands of years ago. But this long-held view about “race” has just in the last few years been proven wrong—and the critique of concepts of race that the new data provide is very different from the classic one that has been developed by anthropologists over the last hundred years. A great surprise that emerges from the genome revolution is that in the relatively recent past, human populations were just as different from each other as they are today, but that the fault lines across populations were almost unrecognizably different from today.

Ancient DNA should be liberating to archaeologists because with answers to these questions in reach, archaeologists can get on with investigating what they have always been at least as interested in, which is why the changes occurred.

Ouch

Regardless of how important FOXP2 itself is in modern human biology, Pääbo cites the search for the genetic basis for modern human behavior as a justification for sequencing the genomes of archaic humans.

Because we need one

The sad truth is that it is possible to count on the fingers of two hands the examples like FOXP2 of mutations that increased in frequency in human ancestors under the pressure of natural selection and whose functions we partly understand. In each of these cases, the insights only came from years of hand-to-hand combat with life’s secrets by graduate students or postdoctoral scientists making engineered mice or fish, suggesting that it will take an evolutionary Manhattan Project to understand the function of each mutation that we have and that Neanderthals do not.

The power of tracing this multitude of lineages to reveal the past is extraordinary. In my mind’s eye, when I think of a genome, I view it not as a thing of the present, but as deeply rooted in time, a tapestry of threads consisting of lines of descent and DNA sequences copied from parent to child winding back into the distant past. Tracing back, the threads wind themselves through ever more ancestors, providing information about population size and substructure in each generation. When an African American person is said to have 80 percent West African and 20 percent European ancestry, for example, a statement is being made that about five hundred years ago, prior to the population migrations and mixtures precipitated by European colonialism, 80 percent of the person’s ancestral threads probably resided in West Africa and the remainder probably lived in Europe. But such statements are like still frames in a movie, capturing one point in the past. An equally valid perspective is that one hundred thousand years ago, the vast majority of lineages of African American ancestors, like those of everyone today, were in Africa.

The evidence for this is that the density of mutations separating San genomes from non-San genomes is uniformly high, implying few shared ancestors between San and non-San in the last hundred thousand years. “Pygmy” groups from Central African forests harbor ancestry that is arguably just as distinctive. The extremely ancient isolation of some pairs of human populations from each other conflicts with the idea that a single mutation essential to distinctively modern human behavior occurred shortly before the Upper Paleolithic and Later Stone Age. A key change essential to modern human behavior in this time frame would be expected to be at high frequency in some human populations today—those that descend from the population in which the mutation occurred—and absent or very rare in others. But this seems hard to reconcile with the fact that all people today are capable of mastering conceptual language and innovating their culture in a way that is a hallmark of modern humans.

Our results do not completely rule out the hypothesis of a single critical genetic change. There is a small fraction of the genome that contains complicated sequences that are difficult to study and that was not included in our survey. But the key change, if it exists, is running out of places to hide. The time scale of human genetic innovation and population differentiation is also far longer than mitochondrial DNA and other genetic data suggested prior to the genome revolution. If we are going to try to search the genome for clues to what makes modern humans distinctive, it is likely that we cannot look to explanations involving one or a few changes.

These examples demonstrate that by leveraging the power of the whole genome to examine thousands of independent positions in the genome simultaneously, it is possible to get beyond the barrier that Molly Przeworski had identified—“Przeworski’s Limit”—by taking advantage of information that we now have about a large number of genetic variations at many locations in the genome that have similar biological effects. We have such information from “genome-wide association studies,” which since 2005 have collected data from more than one million people with a variety of measured traits, thereby identifying more than ten thousand individual mutations that occur at significantly elevated frequency in people with particular traits, including height.

But even if genetic changes—through coordinated natural selection on combinations of many mutations simultaneously—did enable new cognitive capacities, this is a very different scenario from Klein’s idea of a genetic switch. Genetic changes in this scenario are not a creative force abruptly enabling modern human behavior, but instead are responsive to nongenetic pressures imposed from the outside. In this scenario, it is not the case that the human population was unable to adapt because no one carried a mutation that allows a biological capability not previously present. Instead, the genetic formula that may have been necessary to drive the striking advances in human behavior and capacities that occurred during the Upper Paleolithic and Later Stone Ages is not particularly mysterious. The mutations necessary to facilitate modern human behavior were already in place, and many alternative combinations of these mutations could have increased in frequency together due to natural selection in response to changing needs imposed by the development of conceptual language or new environmental conditions. This in turn could have enabled further changes in lifestyle and innovation, in a self-reinforcing cycle.

Today, our closest living relatives are the African apes: the chimpanzees, bonobos, and gorillas, all incapable of making sophisticated tools or using conceptual language.

Argh

With this approach, we found that at least some Neanderthal-related genetic material came into the ancestors of present-day non-Africans eighty-six thousand to thirty-seven thousand years ago.20 We have since refined this date by analyzing ancient DNA from a modern human from Siberia who, radiocarbon dating studies show, lived around forty-five thousand years ago. The stretches of Neanderthal-derived DNA in this individual are on average seven times larger than the stretches of Neanderthal-derived DNA in modern humans today, confirming that he lived much closer to the time of Neanderthal mixture. His proximity in time to the mixing event makes it possible to obtain a more accurate date of fifty-four thousand to forty-nine thousand years ago.

wasn’t convinced by this argument. Rather than low hybrid fertility, I favored the explanation that there simply wasn’t much interbreeding for social reasons. Even today, many groups of modern humans keep largely to themselves because of cultural, religious, or caste barriers. Why should it have been any different for modern humans and Neanderthals when they encountered one another?

Since two changes are required to produce such an incompatibility, the rate of infertility increases with the square of population separation time, so a ten-times-larger population separation translates to one hundred times more genetic incompatibility. In light of this the lack of infertility in hybrids of present-day humans may no longer seem so surprising.

However, the anthropologist Yousuke Kaifu pointed out in a talk I attended in 2011 that the hypothesis of interbreeding near the islands is difficult to square with an absence of archaeological artifacts in the region that could plausibly reflect the presence of a big-brained cousin of Neanderthals and modern humans.

So much being guessed

However, even with the uncertainty about the mutation rate, we can estimate relative dates reasonably well, and we can be confident that this previously unsampled human population split off at about twice the separation time of Denisovans, Neanderthals, and modern humans. I think of this group as “superarchaic” humans, as they represent a more deeply splitting lineage than Denisovans. They are what I call a “ghost” population, a population we do not have data from in unmixed form, but whose past existence can be detected from its genetic contributions to later people.

It is easy to get ensnared in trying to establish neat correlations between genetic dates and the archaeological record, only to have dates shift when a new genetic estimate of the rate of occurrence of new mutations comes along, causing the whole intellectual edifice to come tumbling down.

We called this proposed new population the “Ancient North Eurasians.” At the time we proposed them, they were a “ghost”—a population that we can infer existed in the past based on statistical reconstruction but that no longer exists in unmixed form. The Ancient North Eurasians would without a doubt have been called a “race” had they lived today, as we could show that they must have been genetically about as differentiated from all other Eurasian populations who lived at the time as today’s “West Eurasians,” “Native Americans,” and “East Asians” are from one another. Although they have not left unmixed descendants, the Ancient North Eurasians have in fact been extraordinarily successful. If we put together all the genetic material that they have contributed to present-day populations, they account for literally hundreds of millions of genomes’ worth of people. All told, more than half the world’s population derives between 5 percent and 40 percent of their genomes from the Ancient North Eurasians.

The case of the Ancient North Eurasians showed that while a tree is a good analogy for the relationships among species—because species rarely interbreed and so like real tree limbs are not expected to grow back together after they branch5—it is a dangerous analogy for human populations. The genome revolution has taught us that great mixtures of highly divergent populations have occurred repeatedly.6 Instead of a tree, a better metaphor may be a trellis, branching and remixing far back into the past.

Present-day Europeans and Near Easterners are mixed: they carry within them ancestry from a divergent Eurasian lineage that branched from Mal’ta, European hunter-gatherers, and East Asians before those three lineages separated from one another. Lazaridis called this lineage “Basal Eurasian” to denote its position as the deepest split in the radiation of lineages contributing to non-Africans. The Basal Eurasians were a new ghost population, one as important as the Ancient North Eurasians, measured by the sheer number of descendant genomes they have left behind. The extent of the deviations of the Four Population Test away from the value of zero that would be expected if the populations were related by a simple tree indicates that this ghost population contributed about a quarter of the ancestry of present-day Europeans and Near Easterners. It also contributed comparable proportions of ancestry to Iranians and Indians.

A hint about the possible homeland of the Basal Eurasians comes from the Natufians, hunter-gatherers who lived after around fourteen thousand years ago in the southwestern parts of the Near East.14 They were the first people known to have lived in permanent dwellings—they did not migrate from place to place searching for food despite being hunter-gatherers. They built large stone structures and actively managed local wild plants before their successors became full-fledged farmers. Their skulls as well as the stone tools they made are similar in shape to those of North Africans who lived around the same time, and it has been suggested on this basis that the Natufians migrated to the Near East from North Africa.15 In 2016, my laboratory published ancient DNA from six Natufians from Israel, and we found that they share with early Iranian hunter-gatherers the highest proportions of Basal Eurasian ancestry in the Near East.

Fu’s analysis indicated that most of their ancestry derived from the same sublineage of European hunter-gatherers as the thirty-seven-thousand-year-old individual from far eastern Europe, and that they then spread west, displacing the sublineage associated with Aurignacian tools and represented in the thirty-five-thousand-year-old Belgian individual. The changes in artifact styles associated with the rise of the Gravettian culture were thus driven by the spread of new people.

The data once again showed a correspondence between the archaeological culture and genetic discoveries, documenting the spread of people into central Europe who were not directly descended from the Gravettians who had preceded them. There was also a surprise: most of the ancestry of individuals associated with the Magdalenian culture came from the sublineage represented by the thirty-five-thousand-year-old individual from Belgium who was associated with Aurignacian tools but who was later succeeded at the same site by people who used Gravettian tools and carried DNA similar to others in Europe associated with that culture of eastern European origin. Here was yet another ghost population that contributed to later groups in mixed form. The Aurignacian lineage had not died out, but instead had persisted in some geographic pocket, possibly in western Europe, before its resurgence at the end of the ice age.

After around fourteen thousand years ago, a group of hunter-gatherers spread across Europe with ancestry quite different from that of the people associated with the preceding Magdalenian culture, whom they largely displaced. Individuals living in Europe between thirty-seven thousand and fourteen thousand years ago were all plausibly descended from a common ancestral population that separated earlier from the ancestors of lineages represented in the Near East today. But after around fourteen thousand years ago, western European hunter-gatherers became much more closely related to present-day Near Easterners. This proved that new migration occurred between the Near East and Europe around this time. We do not yet have ancient DNA from the period before fourteen thousand years ago from southeastern Europe and the Near East.

Today, the peoples of West Eurasia—the vast region spanning Europe, the Near East, and much of central Asia—are genetically highly similar. The physical similarity of West Eurasian populations was recognized in the eighteenth century by scholars who classified the people of West Eurasia as “Caucasoids” to differentiate them from East Asian “Mongoloids,” sub-Saharan African “Negroids,” and “Australoids” of Australia and New Guinea. In the 2000s, whole-genome data emerged as a more powerful way to cluster present-day human populations than physical features.

We and another research group32 found that the degree of genetic differentiation between the first farmers of the western part of the Near East (the Fertile Crescent, including Anatolia and the Levant) and the first farmers of the eastern part (Iran) was about as great as the differentiation between Europeans and East Asians today. In the Near East, the expansion of farming was accomplished not just by the movement of people, as happened in Europe, but also by the spread of common ideas across genetically very different groups.

Spurred by the revolutionary technology of plant and animal domestication, which could support much higher population densities than hunting and gathering, the farmers of the Near East began migrating and mixing with their neighbors. But instead of one group displacing all the others and pushing them to extinction, as had occurred in some of the previous spreads of hunter-gatherers in Europe, in the Near East all the expanding groups contributed to later populations. The farmers in present-day Turkey expanded into Europe. The farmers in present-day Israel and Jordan expanded into East Africa, and their genetic legacy is greatest in present-day Ethiopia. Farmers related to those in present-day Iran expanded into India as well as the steppe north of the Black and Caspian seas. They mixed with local populations there and established new economies based on herding that allowed the agricultural revolution to spread into parts of the world inhospitable to domesticated crops. The different food-producing populations also mixed with one another, a process that was accelerated by technological developments in the Bronze Age after around five thousand years ago. This meant that the high genetic substructure that had previously characterized West Eurasia collapsed into the present-day very low level of genetic differentiation by the Bronze Age.

The association between steppe genetic ancestry and people assigned to the Corded Ware archaeological culture through graves and artifacts is not simply a hypothesis. It is now a proven fact.

Is it possible that the steppe people had picked up the plague and built up an immunity to it, and then transmitted it to the immunologically susceptible central European farmers, causing their numbers to collapse and thereby clearing the way for the Corded Ware culture expansion? This would be a great irony. One of the most important reasons for the collapse of Native American populations after 1492 was infectious diseases spread by Europeans who plausibly had built up some immunity to these diseases after thousands of years of exposure as a result of living in close proximity to their farm animals. But Native Americans, who by and large lacked domesticated animals, likely had much less resistance to them. Was it possible that, in a similar way, northern European farmers after five thousand years ago were decimated by plagues brought from the east, paving the way for the spread of steppe ancestry through Europe?

It turns out that the discredited idea of the “Beaker Folk” was right for Britain, although wrong as an explanation for the spread of the Bell Beaker culture over the European continent as a whole.

The Anatolian hypothesis has lost its best evidence, and the most common version of the steppe hypothesis—which suggests that the ultimate origin of all Indo-European languages including ancient Anatolian languages was in the steppe—has to be modified too. DNA has emerged as central to the new synthesis of genetics, archaeology, and linguistics that is now replacing outdated theories.

Some historians of India have thrown up their hands and discounted genetic information due to these apparently conflicting findings. The situation has not been helped by the fact that geneticists do not have formal training in archaeology, anthropology, and linguistics—the fields that have dominated the study of human prehistory—and are prone to make elementary mistakes or to be tripped up by known fallacies when summarizing findings from those fields. But it is foolhardy to ignore genetics. We geneticists may be the barbarians coming late to the study of the human past, but it is always a bad idea to ignore barbarians. We have access to a type of data that no one has had before, and we are wielding these data to address previously unapproachable questions about who ancient peoples were.

Nice summary if the problem

The genetic data also hinted at the social status of the ancient ANI (higher social status on average) and ASI (lower social status on average). Groups of traditionally higher social status in the Indian caste system typically have a higher proportion of ANI ancestry than those of traditionally lower social status, even within the same state of India where everyone speaks the same language.23 For example, Brahmins, the priestly caste, tend to have more ANI ancestry than the groups they live among, even those speaking the same language. Although there are groups in India that are exceptions to these patterns, including well-documented cases where whole groups have shifted social status,24 the findings are statistically clear, and suggest that the ANI-ASI mixture in ancient India occurred in the context of social stratification.

The discrepancy between the Y-chromosome and mitochondrial DNA patterns initially confused historians.26 But a possible explanation is that most of the ANI genetic input into India came from males. This pattern of sex-asymmetric population mixture is disturbingly familiar. Consider African Americans. The approximately 20 percent of ancestry that comes from Europeans derives in an almost four-to-one ratio from the male side.27 Consider Latinos from Colombia. The approximately 80 percent of ancestry that comes from Europeans is derived in an even more unbalanced way from males (a fifty-to-one ratio).

What the data were showing us was that the genetic distinctions among jati groups within India were in many cases real, thanks to the long-standing history of endogamy in the subcontinent. People tend to think of India, with its more than 1.3 billion people, as having a tremendously large population, and indeed many Indians as well as foreigners see it this way. But genetically, this is an incorrect way to view the situation. The Han Chinese are truly a large population. They have been mixing freely for thousands of years. In contrast, there are few if any Indian groups that are demographically very large,

India, of course, has far more people who belong to groups that experienced strong bottlenecks, as the country’s population is huge, and as around one-third of Indian jati groups descend from bottlenecks as strong or stronger than those that occurred in Ashkenazi Jews or Finns.

The people who were custodians of Indo-European language and culture were the ones with relatively more steppe ancestry, and because of the extraordinary strength of the caste system in preserving ancestry and social roles over generations, the ancient substructure in the ANI is evident in some of today’s Brahmins even after thousands of years. This finding provides yet another line of evidence for the steppe hypothesis, showing that not just Indo-European languages, but also Indo-European culture as reflected in the religion preserved over thousands of years by Brahmin priests, was likely spread by peoples whose ancestors originated in the steppe.

How could humans have gotten south of the ice sheets before the ice-free corridor was open? During the peak of the ice age, glaciers projected right into the sea, creating a barrier more than a thousand kilometers in length along the western seaboard of Canada. But in the 1990s, geologists and archaeologists, reconstructing the timing of the ice retreat, realized that portions of the coast were ice-free after sixteen thousand years ago. There are no known archaeological sites along the coast from this period, as sea levels have risen more than a hundred meters since the ice age, submerging any archaeological sites that might have once hugged the shoreline. The absence of archaeological evidence for human occupation along the coast in this period is therefore not evidence that there was no such occupation in the past. If the coastal route hypothesis is right, humans could have walked at that time or later (but still in time to reach Monte Verde) along ice-free stretches of the coastline, possibly bypassing ice-covered sections with boats or rafts, and arriving south of the ice millennia before the interior ice-free corridor opened.

Failure of imagination

Modern genomics offers an unexpected way to recover the past. African Americans—another population that has had its history stolen as its ancestors descend from people kidnapped into slavery from Africa—are at the forefront of trying to use genetics to trace roots. But if individual Native Americans often express a great interest in their genetic history, tribal councils have sometimes been hostile. A common concern is that genetic studies of Native American history are yet another example of Europeans trying to “enlighten” them. Past attempts to do so—for example, by conversion to Christianity or education in Western culture—have led to the dissolution of Native American culture. There is also an awareness that some scientists have studied Native Americans to learn about questions of interest primarily to non–Native Americans, without paying attention to the interests of Native Americans themselves.

Scientists interested in studying genetic variation in Native American populations feel frustrated with this situation. I understand something of the devastation that the coming of Europeans and Africans to the Americas wrought on Native American populations, and its effects are also evident everywhere in the data I and my colleagues analyze. But I am not aware of any cases in which research in molecular biology including genetics—a field that has arisen almost entirely since the end of the Second World War—has caused major harm to historically persecuted groups. Of course, there have been well-documented cases of the use of biological material in ways that may not have been appreciated by the people from whom it was taken, not just in Native Americans. For example, the cervical cancer tumor cells of Henrietta Lacks, an African American woman from Baltimore, were distributed after her death, without her consent and without the knowledge of her family, to thousands of laboratories around the world, where they have become a mainstay of cancer research.15 But overall there is an argument to be made that modern studies of DNA variation—not just in Native Americans, but also in many other groups including the San of southern Africa, Jews, the Roma of Europe, and tribal or caste groups from South Asia—are a force for good, contributing to the understanding and treatment of disease in these populations, and breaking down fixed ideas of race that have been used to justify discrimi...

This is ironic

wonder if the distrust that has emerged among some Native Americans might be, in the balance, doing Native Americans substantial harm. I wonder whether as a geneticist I have a responsibility to do more than just respect the wishes of those who do not wish to participate in genetic research, but instead should make a respectful but strong case for the value of such research.

S

There is a general issue here about the ethical responsibilities of genetic research. When I examine an individual’s genome, I learn not only about the genome of the individual, but also about those of his or her family, and ancestors. I also learn about other members of the community—other descendants of those same ancestors. What are my responsibilities here? What do I owe not only to close relatives of the individual I study, but also to other more distantly related members of their family, to their population, and to our species as a whole? An extreme position that everyone needs to be consulted would make scientific progress in human genetics (including genetic medicine) nearly impossible. There would not be enough time for scientists in modest-sized laboratories like mine to talk with every tribal group that might be interested in the work.

MIssing the point

From my experience interacting with archaeologists, anthropologists, and museum directors who focus on Native American prehistory, it is clear to me that many feel a deep sense of loss about the return of collections of scientifically important bones, and wish to keep them in the possession of museums while acknowledging the dubious ways in which many of these collections were assembled in the course of U.S. expropriation of Native American lands.

At the time of this writing, our knowledge of East Asian population history is relatively limited compared to that of West Eurasia because less than 5 percent of published ancient DNA data comes from East Asia. The difference reflects the fact that ancient DNA technology was invented in Europe, and it is nearly impossible for researchers to export samples from China and Japan because of government restrictions or a preference that studies be led by local scientists. This has meant that these regions have missed out on the first few years of the ancient DNA revolution.

Because Denisovans were so divergent from modern humans, mixture from them could cause Europeans to share more mutations with Chinese than with Australian Aborigines. Indeed, this explained the findings. My laboratory showed that after accounting for Denisovan mixture, Europeans do not share more mutations with Chinese than with Australians, and so Chinese and Australians derive almost all their ancestry from a homogeneous population whose ancestors separated earlier from the ancestors of Europeans.

The Austronesian expansion to the west was equally impressive, reaching Madagascar off the coast of Africa nine thousand kilometers to the west of the Philippines at least thirteen hundred years ago, and explaining why almost all Indonesians today as well as people from Madagascar speak Austronesian languages.

Doesn't use impressed for European peoples

This proof of interaction between highly divergent peoples puts the ball back into the court of archaeologists to explain the nature and effects of those migrations.

While we are beginning to have a relatively good idea of what happened in Europe, Europe does not provide a good road map for what to expect for East Asia because it was peripheral to some of the great economic and technological advances of the last ten thousand years, whereas China was at the center of changes like the local invention of agriculture.

In 2016 and 2017, my laboratory published two papers showing that a shared feature of many East African groups, including ones that do not speak Afroasiatic languages, is that they harbor substantial ancestry from people related to farmers who lived in the Near East around ten thousand years ago.

As Peter Ralph and Graham Coop have shown, the multiple origins in Africa of sickle cell mutations and of mutations that allow people to digest cow’s milk imply that the rate of migration among these populations—even in parts of sub-Saharan Africa less than a couple of thousand kilometers from each other—has been extraordinarily low since the need for these mutations arose. As a result, the most efficient way for evolutionary forces to spread beneficial mutations has often been to invent mutations anew rather than to import them from other populations.

When I discussed these findings with the sociologist Orlando Patterson, he pointed out that the fraction of the European ancestry in African Americans that came from males—which if different from half is called “sex bias”—must have been far greater during the time of slavery. Since the civil rights movement in the United States in the mid-twentieth century, cultural changes have caused the sex bias to reverse, with more coupling between black men and white women. If we carried out DNA studies of African American skeletons from a hundred years ago,

Woo hoo a sociologist