Lone Survivors

by Chris Stringer

  Most of that is still science fiction, and perhaps it is for the best that some elements will always remain so. But for the last 10,000 years, selection seems to have been engineering people to cope with massive lifestyle changes. When humans expanded into novel environments over the last 50,000 years, including into rain forests in Africa and new habitats in Eurasia, Australasia, and the Americas, they encountered fresh challenges and had to adapt both physically and culturally. The physical adaptations ranged from gross changes in body size or shape, down to immunological responses to a host of new pathogens. And over the last 20,000 years these have also included distinct mutations in Europe and Asia for depigmentation, to assuage the lower levels of sunlight, as well as the spread of blue eyes in western Eurasia—although this latter change might equally have come from cultural selection.

  Culture, rather than slowing changes in our DNA, may well have provided the means to speed them up. This is the view of a growing number of geneticists and anthropologists, including Henry Harpending, Gregory Cochran, John Hawks, Anna Di Rienzo, Pardis Sabeti, Sharon Grossman, Ilya Shylakhter, and Kevin Laland. They argue that profound changes in human lifestyles over the last 10,000 years—with the moves to pastoralism, agriculture, and urbanization—would have had equally profound evolutionary effects. With the consequent huge increase in human numbers, there are clear parallels with the relationship between demography and innovation: a larger population will not only have more mutations, and more beneficial mutations, but also provide better chances for them to be conserved and disseminated. And the fact that farming also entailed self-induced changes in societies, diets, and environments (not all of them beneficial to everyone) would have ensured that selection remained a powerful force for evolutionary change.

  Ten thousand years ago, as agriculture was taking off in its west and east Asian cradles, the hunter-gatherer populations of the world probably numbered only a few million people, and in many areas they must have been thinly scattered. The estimated figure only 8,000 years later was over 200 million, and following the industrial revolution and the advent of measures like vaccination, our numbers are now soaring toward 10 billion. The huge increase between 10,000 and 2,000 years ago would have ensured a proportionate increase in mutations, including potentially favorable ones, and, provided population density was high (which it was in many agricultural and subsequent urban communities), any genetic changes had the potential to spread rapidly. As people acquired stable food supplies through farming, they settled down in increasingly large communities, but with this change there were also many downsides. Unsanitary living conditions and densely packed communities were ripe for parasites and epidemic diseases like smallpox, cholera, and yellow fever, while the clearance of forests and the use of irrigation led to the spread of malaria across much of the tropics and subtropics. Overreliance on one or two staple foods also meant that the benefits of a broader hunter-gatherer diet were lost, and, for many, hard labor in the fields wore out bodies prematurely. Societies and technologies had to keep up with the changes too. People were thrown together and socializing in larger numbers, with the growth of task specializations, and disparities in wealth, status, and, no doubt, reproductive success.

  An evolutionary tree showing the geographic distribution of humans and humanlike relatives from the last 2 million years. Note the complexity of relationships now implied by the latest genetic data.

  All of these upheavals should have provided fertile ground for evolution to operate, and so many groups of geneticists have been combing the human genome for signs of this. The methods are known as genome-wide or whole-genome association studies, where a correlation is sought between genes and particular traits, whether these are physical, such as skin color or height, or physiological, such as susceptibility to a disease. Of course such studies must take into account environmental influences, as well as the complexity of gene expression, since a particular end result may come from the interaction of several different genes, rather than just one. A major source for association studies has been the International Haplotype Map, which has provided data on millions of SNPs in 270 people of European, Nigerian, Chinese, and Japanese descent. These single letter mutations are inherited within larger sequences of DNA, and segments break down over time as a result of the remixing of the DNA on our chromosomes with every new generation. New mutations can be spotted, and their age can be estimated by the amount of mixing that has occurred around them.

  Sure enough, the signals of recent selection not only were there but were also very strong, acting on perhaps 20 percent of our genes. Some could be directly related to the changes induced by farming, linked to new diets, such as the gene for lactase. This is an enzyme that allows infants to digest lactose (milk sugar) when nursing, but it usually switches off during childhood, so that many adults are lactose-intolerant. However, in the last 10,000 years, separate genetic changes occurred in East Africa and regions of western Eurasia that prevented the lactase gene switching off, meaning that adults (about 80 percent in the case of Europeans) can comfortably digest milk from livestock. Populations elsewhere who lack the mutations, such as East Asians and Native Australians and Americans, are still only able to drink milk comfortably as babies. Meanwhile, mutations have evolved to allow the digestion of other “new” carbohydrates in the diet in West Africa (for the sugar mannose) and East Asia (mannose and sucrose). And there have also been changes in a gene that codes for salivary amylase (which helps to digest starch), both in its structure and in the number of copies of the gene in many individuals. Examples of recent selection in human genes have been known for many years in connection with protection from malaria, and at least twenty-five different examples have now been detected. Because the malarial parasite is transmitted in the bloodstream, many human defenses originate in the blood, such as mutations in the hemoglobin gene, which carries oxygen, or in the enzyme G6PD. And blood groups have responded too, with an entirely new one—Duffy—seemingly selected specifically to combat the disease. Many further changes seem to be related to resistance to infectious diseases such as tuberculosis, and 10 percent of Europeans have been fortuitous in carrying mutations that have apparently been selected to resist smallpox; they also seem to confer resistance to HIV.

  Other recent changes may be related to the changing social conditions brought by agricultural life. In chapter 6, we mentioned mutations in the gene for the cholesterol-transporting apolipoprotein E that seem to lower the risk of many age-related conditions such as coronary disease, and there are at least fourteen other recently mutated genes that are linked with conditions most expressed in the old, such as cancers and Alzheimer’s. Considering the crucial importance of extended families for both hunter-gatherers and farmers, selection seems to have been working on the survival of people past reproductive age as well, given the consequent social benefits. But a possible downside for social harmony from higher population densities is the greater potential for adultery, and this may be reflected in widespread but regionally distinct mutations controlling the quantity and vigor of human sperm—perhaps indicative of “sperm competition,” caused when a woman partners more than one man within a day or so. Perhaps some of the one hundred or so recent mutations in brain neurotransmitters concerned with mood and demeanor have correspondingly been selected to cope with the social consequences of our large population numbers and the possible resultant tensions.

  Those neurotransmitters are only a part of our changing genome as far as the brain and senses are concerned. Although this is a highly controversial area, it is likely that selection has favored different behaviors and cognitive abilities as modern humans have diversified in different environments and social complexities. With the development of specialized occupations and their associated skills, selection may have increasingly come into play. For example, the need to work out stocks of cereals or animals, followed by the rise of trading and the arrival of money, would all have encouraged selection for mathematical abilities. And the increasing
complexity of communication in small or ever-larger groups may be marked by recent mutations in genes that produce proteins for the cilia of our inner ears and the membrane that coats them, as well as one that helps to build the actual bones of the middle ear, which transmits sonic frequencies. The fact that different mutations are found when comparing Chinese and Japanese, Europeans and Africans suggests that selection might even have been tracking the evolution of different languages and their most characteristic sounds. Sight, too, may have been under recent selection in East Asia—mutations in the protocadherin-15 gene there affect the workings of both inner ear cells and photoreceptors in the retina.

  But to return to the question posed earlier, it appears that human evolution, at least in terms of changes in individual DNA sequences, has accelerated rather than slowed or stopped over the last 10,000 years. Indeed, some calculations suggest that it is now happening a hundred times faster than it did since we split from the lineage of chimpanzees, probably more than 6 million years ago. About 7 percent of human genes seem to have mutated recently in some populations, the majority within the last 40,000 years, and particularly within the last 10,000 years. Some caution has to be injected here, since geneticists like Sarah Tishkoff and Mark Stoneking have pointed out that the expansion of human populations might have increased rare variants by chance alone, so the functional benefit of the genetic change needs to be properly demonstrated—as it can be in many cases. Additionally, and perhaps more seriously, the constant loss and overwriting of changes in our DNA mean that some ancient signals of genetic change—during the Middle Stone Age, for example—have been lost or are difficult to detect now. Thus we have a biased signal for the last 10,000 years or so, because this is the very period when we have the most chance of recognizing novel mutations.

  Fortunately this is a fast-moving area of science, and a lot of new data will be arriving to resolve this question in the next few years—including a thousand complete human genomes from around the world. Pardis Sabeti, as well as singing in a rather good rock band, has worked with her colleagues on a new method that combines three tests for multiple signals of selection, and which has the potential to increase the resolution of scans for recently selected DNA as much as a hundredfold. She is also researching something important that we haven’t touched on—not every genetic change involves our DNA. Ribonucleic acid (RNA), like DNA, consists of long chains of nucleotides, but these chains are usually single-stranded in our cells. Different types of RNA are central to protein synthesis and to the regulation of gene expression, and thus RNA—which also mutates—forms another subject and agent of evolutionary change. This is part of a growing body of data concerning inheritance that lies beyond the genetic code of DNA, constituting the field of epigenetics (from the Greek, meaning “over or above genetics”). This is a fast-developing area of research that will not replace the current focus on DNA, but certainly provides additional ways of looking at inheritance and evolution. Here, short-term environmental changes may have an impact on bodily form and function beyond changes purely in our DNA—for example, via histone proteins that make up part of the chromosomes, or through the modifications that viruses or prions may inflict on us.

  Finally, although this discussion of recent changes in human DNA has constantly referred to selection, we should bear in mind that selective changes may not benefit everyone; there can be winners and losers, as there has been with the rise of sickle-shaped cells in the blood of African-derived populations. Sickling has benefited those who are heterozygous for the sickle-cell gene (that is, they have only one copy of it) by conferring some immunity against the malarial parasite. But without medical intervention, those born with two copies of the gene will be highly anemic and will die prematurely. The frequency of a mutation in the leptin receptor gene has increased dramatically in East Asia, linked with changes in the body mass index and a tendency to store fat. This may have been beneficial for adaptation to colder climates but now is a cause of high blood pressure and obesity. Some researchers have also argued that long and stressful sea voyages, whether forced in the case of the slave trade or voluntary in the case of the colonization of Polynesian islands, would have selected physiques and physiologies that were best able to survive the rigors of those journeys. The survivors then went on to found much larger populations who now live under very different conditions, perhaps explaining the prevalence of salt-sensitive hypertension in American blacks, and of diabetes and obesity in parts of Oceania. Similarly, as the anthropologist Peter Ellison pointed out, it is possible that the apparent increasing frequency of conditions like autism, schizophrenia, allergies, asthma, autoimmune diseases, and reproductive cancers are the modern downside of genetic changes that were beneficial under more ancient human environments and lifestyles. These comparisons between the past and the present are the basis of a whole new field of science called evolutionary medicine.

  It is not always clear what the precise agent of selection has been in the past, beyond differential reproductive success. Where disease is concerned, it is obvious that this will cause direct natural selection through the reduced fertility or death of those whose natural (inherited) defenses are unable to cope with the condition in question. But exposure to the pathogens may be reduced or increased by particular human behaviors (think of the use of condoms, which act as contraceptives, but also combat the spread of HIV). Thus many of these changes probably lie in the realm of complex interactions between the natural environment and ones we have created through our diversity of human cultures. And this brings us back to one of Darwin’s favored evolutionary mechanisms, as highlighted by the full title of his second most famous book: The Descent of Man, and Selection in Relation to Sex. It is evident that, as Darwin proposed, some of these changes could be ascribed to human sexual/cultural selection, where habitual preferences in mating could steer evolution in a particular direction. This might well include some of the regional (“racial”) differences in appearance, as Darwin suspected, and equally some of the changes in brains and behavior. Stature is a case in point; it is a complex trait, but one with a high heritability. There is evidence that stature (as long as it does not become excessive) is linked to both fecundity and wealth in the developed world, and studies of the selection of sperm donors suggest that women prefer taller donors, which will in turn lead to taller offspring.

  All of this would have fascinated Darwin. When he was alive, the hard data about our origins could have been packed up in a small suitcase, and while in many ways he started the writing of the book of human evolution, all he could achieve was the equivalent of drafting some chapter titles and words and sentences scattered through it. Since then we have learned so much about our early history, and many more words, sentences, and paragraphs of our story are now in place. Some chapters are fairly complete, such as the ones about building complete human and chimpanzee genomes, with the Neanderthal and Denisovan chapters following now. And yet the writing of other chapters has hardly begun, such as the ones about how our brains really work, who were the first peoples of the Indian subcontinent, the early history of the Hobbit in southeast Asia, and who was living in West Africa for most of prehistory.

  Certainly, until we have a dated fossil, archaeological, and environmental record from many more regions to match the quality of the ones we have from western Europe, and are beginning to have from places like eastern and southern Africa, we cannot even guess how the book of our evolutionary history will look when it nears completion. Paleoanthropology is such a fast-moving and fast-developing science that even some of what is already written in that book will need to be corrected, or perhaps even deleted altogether, including my own contributions, no doubt. The process of writing this book has led me to a greater recognition of the forces of demography, drift, and cultural selection in recent human evolution than I had considered before. And while I have been writing it, new genetic data have emerged to show that we Homo sapiens are not purely derived from a recent African origin. But this dynamis
m is what makes studying human evolution so fascinating, and science is not about being right or wrong, but about gradually approaching truth about the natural world.

  When Darwin died and was granted the honor of being buried in Westminster Abbey, there were many rich tributes to the man and his work, as this example shows.

  Mr. Darwin has left as broad and deep a mark upon Psychology as he has upon Geology, Botany, and Zoology. Groups of facts which previously seemed to be separate, are now seen to be bound together in the most intimate manner; and some of what must be regarded as the first principles of the science, hitherto unsuspected, have been brought to light. If the proper study of mankind is man, Mr. Darwin has done more than any other human being to further the most desirable kind of learning, for it is through him that humanity in our generation has first been able to begin its response to the precept of antiquity—know thyself.

  That last phrase harks back to ancient Greece but was also Linnaeus’s directive in describing the species he named Homo sapiens. Knowing thyself, for me, has meant a journey from measuring fossil skulls in European museums forty years ago to looking at almost every aspect of our origins. Knowing ourselves has meant recognition that becoming “modern” is the path we perceive when looking back on our own evolutionary history. That history seems special to us, of course, because we owe our very existence to it. Those figures of human species (usually males) marching boldly across the page have illustrated our evolution in many popular articles, but they have wrongly enshrined the view that evolution was simply a progression leading to us, its pinnacle and final achievement. Nothing could be further from the truth. There were plenty of other paths that could have been taken; many would have led to no humans at all, others to extinction, and yet others to a different version of “modernity.” We can only inhabit one version of being human—the only version that survives today—but what is fascinating is that paleoanthropology shows us those other paths to becoming human, their successes and their eventual demise, whether through failure or just sheer bad luck. Sometimes the difference between failure and success in evolution is a narrow one, and we are certainly on a knife edge now as we confront an overpopulated planet and the prospect of global climate change on a scale that humans have never faced before. Let’s hope our species is up to the challenge.