The complicated origins of our species

Abstract

Advanced methods of sequencing ancient DNA provide unprecedented insights into the origins of our species, adding up to a much more complex picture than previously established models suggested. Michael Gross reports. Advanced methods of sequencing ancient DNA provide unprecedented insights into the origins of our species, adding up to a much more complex picture than previously established models suggested. Michael Gross reports. The ritual rooms of the Pueblo culture in North America, known as kiva, typically contain a hole in the ground, the sípapu. It symbolically represents the origin of the tribe, the passage through which its people first came into this world. Creation myths in other cultures, like the biblical one of the Garden of Eden, also like to pin down the origin of mankind to one place and one event, even if the place may be out of our reach. The scientific study of the origins of our species has over the last few decades very successfully focused on the ‘Out of Africa’ model, which posits that Homo sapiens arose between 200,000 and 150,000 years ago in sub-Saharan Africa. Migrating out of Africa to Eurasia between 60,000 and 80,000 years ago, it spread around the world and successfully replaced archaic populations such as Homo erectus and the Neanderthals, who had migrated out of Africa at earlier times. The quest to establish specific details of this population history has often been framed in terms derived from the genesis. Thus, Homo sapiens’ native habitat became the Garden of Eden, and efforts to establish genetic characteristics of a founder population were often described as a search for the genes of Adam and Eve. To a certain extent, these apparently unscientific descriptions remained close to the actual results, as mitochondrial DNA, for instance, pointed to a common ancestor, a ‘mitochondrial Eve’ who lived around 200,000 years ago, and the spread of genetic diversity could be traced to specific parts of Africa. With the spectacular developments in recent years delivering the genome sequences of the Neanderthal and a new Homo population, the Denisovans, the story is becoming more and more complicated, however. New archaeological finds in unexpected places are adding to the complexity, and the popular story of a geographically well-defined ‘cradle of mankind’ and a small founder population may turn out to be a simplification, if not another creation myth. In a provocative talk at the recent Cell Symposium Evolution of Modern Humans: From Bones to Genomes at Sitges, Spain, Jean-Jacques Hublin from the Max-Planck Institute for Evolutionary Anthropology at Leipzig, Germany, argued that the dominant models of human origins in Southern and East Africa are flawed due to biased evidence. “The fossil evidence is biased by the streetlight effect,” Hublin said, referring to the widespread inclination of scientists to search for evidence where they can best see. Thus, Hublin mused that the early Homo sapiens populations already respected the frontier between South Africa and Botswana, as maps of archaeological sites seem to suggest. A lot of work is done in South Africa, Hublin said, but virtually none in more difficult places such as Angola or Mali. Moreover, the changing climate means that some of the Savannahs where early humans hunted are now inaccessibly buried under rainforests, while in Northern Africa the expansion of the Sahara displaced or led to extinction ancient hunter-gatherers. Periodically during the last 130,000 years, Hublin argued, the area of today’s Sahara was a savannah with lakes and rivers. In particular, the Aterians archaeological sites (named after the site Bir el-Ater in Algeria) document numerous human settlements between 100,000 and 40,000 years ago. Their remains and artefacts, including body ornaments and projectile points, are best preserved on the margins of today’s desert. They were as advanced as those from the same period from South Africa. This, Hublin argues, suggests connections between populations of human hunter-gatherers across the whole of Africa — a complex situation from which our world-conquering ancestors emerged. At the beginning the last glacial period, arid conditions led to the end of the Aterian culture and their domain has been later re-peopled by non-African groups. “Thus the genomes of the last African hunter-gatherers (Pygmies, Sandawe, Hadza or San) also provide us with a biased picture of the African populations predating the last out-of-Africa exodus,” Hublin concludes. Leaving the beaten track and searching away from the streetlights can pay off for researchers. Pamela Willoughby from the University of Alberta, Edmonton, for instance, says that the Southern Highlands of Tanzania appeared to be an unlikely place to look for Stone Age remains when she started working there in 2008, excavating in two rock shelters that seem to have been in continuous use since the Middle Stone Age. The wealth of material her group has discovered since then in sites around the modern city of Iringa, including the oldest directly radiocarbon-dated ostrich eggshell beads (Miller and Willoughby, J. Human Evol. (2014) in press) suggests that this area served as a refuge during the last Ice Age, when populations in Africa shrank, as has been shown by genetics. Speaking at the same meeting, Chris Stringer from the Natural History Museum at London, UK, agreed that “ideas of a single African centre of origin are probably illusory.” According to Stringer, “it seems more likely that what we recognise as ‘modern humans’ are the result of a composite of DNA, morphology and behaviour derived from a variety of regions and populations across Africa, perhaps even including input from surviving members of the species heidelbergensis.” He referred to this modified view as a “coalescent African origin” (Trends Ecol. Evol. (2014) http://dx.doi.org/10.1016/j.tree.2014.03.001). Part of the problem in elucidating the complex origins of humans in Africa can be assigned to the fact that modern Africans are still underrepresented in genome analysis (Curr. Biol (2011), 21, R481–R484), as Sarah Tishkoff from the University of Pennsylvania, USA, pointed out at the Sitges meeting. Her group is using whole genome SNP genotyping and high coverage sequencing to study genetic diversity in African populations. Specific issues her group has addressed recently include the origins of east Africa click-speaking hunter-gatherers, where evidence suggests that populations in Tanzania have a recent common ancestry with populations from hunter-gatherer populations from Kenya and Ethiopia, the origins of lactose tolerance in Africa and tracing migration of pastoralist populations (Am. J. Hum Genet. (2014) http://dx.doi.org/10.1016/j.ajhg.2014.02.009), as well as the genetic basis of short stature in Pygmies. Further work on lactose tolerance from the groups of Mattias Jakobsson and Mark Stoneking has appeared in this journal online on April 3rd (Curr. Biol. (2014) http://dx.doi.org/10.1016/j.cub.2014.02.041; http://dx.doi.org/10.1016/j.cub.2014.03.027). Beyond these specific questions, African genomics is likely to hold many important clues to the family tree of our species. After all, the fact that Africans are much more genetically diverse than the rest of the world combined is one of the key pieces of evidence for the out of Africa model, and a better understanding of that diversity is bound to bring benefits both for the understanding of our African origins and for current medical problems. It is fairly clear that the ancestors of all non-Africans left Africa some 60,000 years ago, but our views of what happened next have dramatically changed due to the genome sequencing work from Svante Pääbo’s work at Leipzig. Following the whole genome sequence of Neanderthal remains found in Vindija Cave, Croatia, and comparisons with genomes of present-day humans from all continents, Pääbo’s team concluded that the out-of-Africa migrants interbred with Neanderthals (whose ancestors had left Africa much earlier) in the Middle East, before they spread out and headed in different directions to conquer Europe, Asia, Oceania and the Americas. All present-day non-Africans, from Cape Horn to Spitsbergen, share a characteristic Neanderthal heritage of around one to two percent of their DNA. Soon afterwards, an even bigger surprise awaited the researchers in the shape of a now-famous finger bone from a cave in Denisova, Siberia. The genome analysis revealed this relic to be from a girl of a hitherto unknown hominin species, now referred to as Denisovan. Again, genome comparisons showed that Denisovans interbred with Homo sapiens, although their shared descendants are only found in Oceania. Most recently, Pääbo’s group published the high-quality genome sequence of a Neanderthal woman from the same cave that yielded the Denisovan bone, but from an earlier time period (Nature (2014) 505, 43–49). It revealed a surprising level of inbreeding. Her parents shared genes to the same extent as half-siblings, and further inbreeding must have occurred in previous generations. Intriguingly, this new genome in conjunction with the Denisova genome also allowed the detection of gene flow into the Denisovans from a fourth population quite distinct from Neanderthals, Denisovans, and modern humans. As Ewan Birney and Jonathan Pritchard commented in a News and Views piece in Nature, “it does seem that Eurasia during the Late Pleistocene was an interesting place to be a hominin, with individuals of at least four quite diverged groups living, meeting, and occasionally having sex.” Summarising these developments at the Sitges symposium, Pääbo described the population events after the exodus from Africa as a “leaky replacement” of archaic species with the migrating Homo sapiens. Still, as Pääbo has pointed out, the fact that genes have flown into the gene pool of our ancestors suggests that the offspring of mixed Neandertal and modern human ancestry must have been accepted and integrated into modern human populations. What the genomes still don’t tell us is why Neanderthals became extinct some 30,000 years ago (Curr. Biol. (2011) 21, R871–R873). Ultimately, Pääbo’s ambition is to use his unprecedented insights into the genomics of our closest archaic relatives to work out what makes us human. There are only around 31,000 bases in which the human genome consistently differs from the consensus between chimpanzee and Neanderthal. Understanding the significance of these differences, Pääbo hopes, will answer the age-old question of why we are people rather than apes, and why we became so adaptable that we could thrive around the globe. This line of research may lead scientists into further conflict with those people who look to their religion or philosophy for answers to such deep identity questions. Naturally, these issues attract the attention of the general media as well. The Sitges conference had sufficient media reporters in attendance for the organisers to set up a panel discussion on the representation of human evolution in the media. Progress in the analysis of ancient DNA has also revolutionised the genetic investigation into how the small population that came out of Africa managed to spread around the rest of the world. While Svante Pääbo’s group finished the first Neanderthal genome, Eske Willerslev’s team at the University of Copenhagen, Denmark, together with the BGI at Shenzhen, China, completed the first genome of an ancient Homo sapiens, a palaeo-eskimo from the Saqqaq culture in Greenland. The genome was sequenced from a lock of hair preserved in permafrost for around 4,000 years. Since then, Willerslev’s team has sequenced ancient genomes from around the world, allowing long-awaited experimental verification of the hitherto speculative hypotheses about the peopling of the continents. In recent work regarding the population history of the Americas, Willerslev and colleagues have sequenced the genome of a boy who lived in Mal’ta in south-central Siberia 24,000 years ago (Nature (2014) 505, 87–91). They found that the boy was more closely related to Native Americans and Europeans than to today’s inhabitants of East Asia. The results suggest that the ancestors of modern Europeans expanded further east than previously thought and that they contributed between 14 and 38% of the genetic heritage of Native Americans. The most likely scenario for the settlement of the Americas is that a population from Siberia arrived in northwestern Beringia (the area of today’s Bering Strait) around 32,000 years ago. Between 26,000 and 18,000 years ago, these populations expanded into the eastern part of that area, arriving in what is now Alaska, and evolving characteristics that are now shared by Native American populations. At that point, the ice shield stretching across Canada blocked their progress southwards, but 17,000 years ago the Pacific coastline became ice-free and passable, such that the first Americans could expand. Within a few thousand years their descendants reached South America. A key group of archaeological finds relating to the early migration into North America is the Clovis culture, dated to 13,000 to 12,600 years ago. Recently, Willerslev’s lab reported the genome sequence of the only human skeleton associated with the Clovis culture, a young boy found at the Anzick site in Montana (Nature (2014) 506, 225–229). The genome sequence essentially confirms the widely held belief that the Clovis culture represents the migrant population that spread out across the Americas. This leaves no space for some of the more speculative alternative explanations linking the artefacts to hypothetical invasions from Europe. In his work in Native American genomics as well as in his earlier studies with Australian Aborigines, Willerslev places a lot of emphasis on explaining the nature of the work to the indigenous peoples, to ensure that they don’t feel tricked or robbed. In the case of the Clovis boy, the US Native American Graves Protection and Repatriation Act, does not apply, as the boy’s remains had been discovered on private land. Still, Willerslev teamed up with the academic Shane Doyle from the Crow tribe to visit nearby tribes who may feel they are related to the boy, and to ask their permission for the publication of the genome. Speaking directly to the Native Americans, Willerslev reports that he generally found good understanding and no major objections to the publication. As Willerslev explained at the Sitges symposium, he found it important also to listen to the views of the Native tribes regarding their origins and ancestors. Offering the insights of science as an additional tool to find out about their ancestors, rather than asking them to drop their traditional beliefs, seems to have enabled harmonious relations so far, in contrast to earlier cases in the 1990s, where conflicts erupted over human remains and scientists ended up losing the opportunity to study them. Also, the myths and legends may contain a grain of useful information for the scientists as well, for instance in preserving the memories of certain environmental conditions or changes of conditions, such as lands of plenty or sudden floods. And if geneticists speak of population bottlenecks that we have come through, the symbolic hole in the ground of the kiva isn’t so far removed from our scientific metaphor.