The Neanderthal within

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1 Record: 1 Title: Authors: Source: Document Type: Subject Terms: Geographic Terms: Abstract: Lexile: Full Text Word Count: ISSN: Accession Number: Database: Section: Features The Neanderthal within. Jones, Dan New Scientist, 3/3/2007, Vol. 193 Issue 2593, p28-32, 5p Article HUMAN remains (Archaeology) ANTHROPOLOGY HYBRIDIZATION NEANDERTHALS EUROPEANS ZILHAO, Joao LAGAR Velho Rockshelter (Portugal) PORTUGAL The article discusses the possibility of interbreeding among early Europeans and Neanderthals. Topics include an overview of the 24,000-year old Lagar Velho child found by anthropologist João Zilhão in Lagar Velho, Portugal, thought to be a Neanderthal hybrid. Also discussed is the role interbreeding may have played in human evolution, the single origin model, and comments by Erik Trinkaus, an expert on Stone Age humans who performed tests on the Lagar Velho child MasterFILE Premier The Neanderthal within Did our ancestors interbreed with other species of human? We might be more of a hybrid than we'd care to believe, says Dan Jones AFTER the boy died, he was buried in a shallow grave along with some pierced shells and red ochre, as was customary among his people. There he lay for 24,000 years until his nearcomplete remains were unearthed by anthropologist João Zilhão at Lagar Velho in Portugal. He was expecting to find the remains of an early modern human -- Neanderthals were thought to be long extinct by that time -- but the boy's skeleton was different. Realising that he had something unusual and potentially significant on his hands, Zilhão called in Erik Trinkaus, an expert on Stone Age humans at Washington University in St Louis, Missouri. In 1999, Trinkaus and Zilhão, who is at the University of Bristol in the UK, published their 1/8

2 analysis of the Lagar Velho child. They argued that his bones provided the answer to a longstanding and delicate question about human evolution: did our ancestors interbreed with Neanderthals? The child, the team argued, was clearly a human--neanderthal hybrid. He had the prominent chin and facial features of a Cro-Magnon, but also the stocky body and short legs of a Neanderthal. The only possible explanation was that he was the product of long and extensive interbreeding between early Europeans and the Neanderthals. This interpretation was -- and still is -- controversial. While the possibility of interbreeding between our direct ancestors and other human species has long been recognised, there has never been much evidence to support it. Since the discovery of the Lagar Velho child, however, new lines of evidence have started to emerge, largely from genetics but also from new fossils. As the findings stack up, researchers are edging towards the conclusion that interbreeding not only happened, but that it played an important role in our evolution. Like it or not, we may have to accept that our species is, to some extent, a hybrid. There's a little bit of Neanderthal in all of us. For the past 20 years the prevailing view of the origin of modern humans has been fairly straightforward. About 160,000 years ago a small, isolated population of archaic humans, most likely in east Africa, evolved the anatomical characteristics that define modern humans. According to this "single origin" or "out of Africa" model, their descendants spread across the globe, completely replacing existing species, such as Neanderthals and Homo erectus, that were widespread at the time. If there was any interbreeding, it was insignificant. That picture replaced an earlier consensus called multiregionalism. Multiregional theories propose that humans evolved towards modernity in a more distributed manner, with modern human genes arising in various sub-populations across Africa and Eurasia and then spreading throughout the entire human population through regular breeding between these sub-populations. Until the mid-1980s most palaeo-anthropologists were multiregionalists, based on fossil evidence hinting at widespread, parallel evolution towards modern forms. Then genetic evidence entered the debate. In 1987, a team led by Allan Wilson of the University of California, Berkeley, published an analysis of mitochondrial DNA (mtdna) sequences from 147 people from five geographically distinct populations. Mitochondria are very useful for tracking evolutionary history: their DNA passes directly down the maternal line, remaining unchanged unless a mutation occurs. Measured over thousands of years, these mutations occur at a regular rate, ticking like a molecular clock. Each new mutation gives rise to a new lineage of mtdna, like the branches on a family tree. By analysing the mtdna sequences of a large number of people, geneticists can build a "gene tree", working backwards in time and eventually converging on a common ancestor. The gene tree can also tell you where the ancestor probably lived. Mitochondrial Eve The one Wilson and colleagues drew up came out strongly in favour of the single origin model. It pointed to a recent common ancestor for all modern humans -- a single woman, the famous Mitochondrial Eve, who lived in Africa about 170,000 years ago. Later studies on the Y 2/8

3 chromosome, which passes exclusively down the male line, told pretty much the same story, converging on a single man -- Y-chromosomal Adam -- who lived about 100,000 years ago. "Subsequent genetic data either backed this up or at least didn't refute it," says Dan Garrigan, an evolutionary geneticist at Harvard University. "By the mid-1990s the 'out of Africa' view had become the dominant view of human evolution," adds Chris Stringer, a palaeontologist at the Natural History Museum, London, and an early proponent of the model. The story told by mtdna and the Y chromosome supports the single origin model, but these are not the only source of genetic information about patterns of human evolution. In terms of size, the nuclear genome dwarfs mtdna and the Y chromosome, making it a potentially richer resource for reconstructing human history. Nuclear DNA is harder to work with, though. Unlike mtdna or the Y chromosome, which are both passed down intact, the nuclear genome is chopped u p and recombined into novel combinations every generation. This genetic shuffling makes it very difficult to build gene family trees: you can't be sure whether sequence differences arose through shuffling or mutation. For a long time that made it all but impossible to derive information on evolutionary history from nuclear DNA. In recent years those hurdles have been overcome. It turns out that there are small chunks of nuclear DNA called haplotypes that tend not to be broken up by recombination, and so, like mtdna, pass from generation to generation intact and can be used to build gene trees. In recent years sequencing technology, and the computational tools for analysing sequence data, have improved to the point where haplotypes can provide useful evidence about human history -- evidence that is at odds with the single origin model. "There are patterns of variation in the genome that don't really fit," says Michael Hammer, an evolutionary geneticist at the University of Arizona in Tucson. The first such odd pattern was discovered in the late 1990s, when anthropologist Eugene Harris and geneticist Jody Hey at Rutgers University in Piscataway, New Jersey, looked at a haplotype within a gene called PDHA1. By sequencing DNA samples taken from 35 men across the world, they found that there were several versions of this haplotype in the modern population. So far, so unsurprising. But when Harris and Hey constructed a gene tree for the sequences, something stood out. They found that the sequences could be clumped into two basic types, or lineages, which last shared a common ancestor a whopping 1.8 million years ago. Then 200,000 years ago one of the lineages split again (Proceedings of the National Academy of Sciences, vol 96, p 3320). But if humans evolved from a small, reproductively isolated group about 160,000 years ago, how could the PDHA1 haplotype have diverged 1.8 million years ago, and again 200,000 years ago? "The pattern is completely incompatible with a model in which modern humans derive from a single population," says Garrigan. In the parlance of population genetics, PDHA1 shows "deep ancestry". This poses a big problem for the single origin model. If the model is correct, all our genes should converge on a single common ancestor who lived fairly recently -- that is, they should show shallow 3/8

4 ancestry. On the whole, they do. But PDHA1 does not, and it isn't alone. "We're repeatedly finding genetic lineages with deep ancestry that stick out from other areas of the genome," says Sarah Tishkoff, an evolutionary geneticist at the University of Maryland in College Park. "The tough part is explaining these patterns." One solution is to revive the multiregional model, which Harris and Hey proposed doing. But there is another, more dramatic explanation: interbreeding. In this model, modern humans did evolve from a single population in Africa, but occasionally acquired genes from other human species by having sex with them. Interbreeding would explain why our genome contains some chunks of DNA with deep ancestry: they evolved in archaic species and "introgressed" into us. If that's true then we are, to some extent, a hybrid species -- a mosaic of "our" genes, Neanderthal genes and possibly even Homo erectus genes too. To some that's a step too far. Surely our direct ancestors would not have been remotely interested in inter-species sex. And even if they were, what are the chances of such dalliances producing viable, fertile offspring? Many experts, however, think human- Neanderthal mixing would have been entirely possible. "They were very closely related, so there could be interbreeding," says Stringer, even though he thinks the biological significance of this is likely to be low. Until recently, the available evidence suggested that there was no interbreeding. All Neanderthal mtdna genomes sequenced so far are distinct from our mtdna. But that still left plenty of scope for finding introgressed genes in the nuclear genome. Last year, dramatic and compelling evidence emerged for this type of gene flow. For the past few years Bruce Lahn, a geneticist at the University of Chicago, has been studying genes potentially involved in human cognition, in particular one called microcephalin. Mutations in microcephalin cause the condition microcephaly, characterised by a small head and various neurological symptoms. Like many genes involved with brain development, microcephalin has evolved rapidly in humans. In previous studies, Lahn showed that one variant of microcephalin appeared about 40,000 years ago and has since swept through the population, propelled by the power of natural selection. The new variant is found in 70 per cent of living people. "We don't yet know exactly what this variant does or why it is being selected for -- it could be something to do with cognition," says Lahn. The obvious interpretation is that the new version arose 40,000 years ago via a chance mutation in the microcephalin gene. Lahn thinks otherwise. In a paper published last year, he looked at a haplotype within microcephalin. On the basis of sequence differences between the old and new versions of the gene, he concluded that the two are so different that they must have diverged at least 1 million years ago (Proceedings of the National Academy of Sciences, vol 103, p 18178). 4/8

5 This combination of deep ancestry on one level and shallow ancestry on another suggests that something very unusual might have happened. It is as if the new version of microcephalin split off from our evolutionary lineage a million years ago, then jumped back in 40,000 years ago. According to Lahn, that is exactly what happened. By far the most likely explanation, he says, is that the newer version of the gene evolved in a separate species of human -- probably Neanderthals -- and then entered our lineage through interbreeding. "These dates roughly correspond to human--neanderthal divergence 1 million years ago, and the time when they coexisted in Europe 40,000 years ago, which naturally leads to the hypothesis that the new microcephalin gene introgressed from Neanderthals to humans," says Lahn. "Once in the human gene pool, the new variant was selectively favoured and now represents about 70 per cent of the worldwide frequency." In this case multiregionalism cannot explain the pattern: the gene is so strongly favoured by natural selection that if it arose in a subpopulation of humans that was in regular sexual contact with others it would have spread throughout our lineage much earlier. There's an irony here. If Lahn is right, a gene potentially underpinning the power of the modern human brain originally arose in Neanderthals, popularly portrayed as our intellectual inferiors. With the Neanderthal genome expected within two years we may have confirmation of this introgression. Microcephalin and PDHA1 are hardly anomalies. "These are just two of a growing list of regions of the genome that do not fit with a strictly single origin model," says Hammer, whose lab has found several other cases and is searching for more. Hammer is taking a different tack from Lahn. Instead of looking at genes like microcephalin, Hammer is concentrating on haplotypes in non-coding, or neutral, regions of the genome -- "junk" DNA that can accumulate mutations without any biological effect. The reason for taking this approach is to move the introgression story another step forward. A gene like microcephalin can tell you that interbreeding probably happened, but it can't tell you how often. Because it has been strongly selected, microcephalin could have entered the human population from a single copy that introgressed 40,000 years ago. In other words, its presence could in theory be the result of the only human--neanderthal sexual encounter ever. Neutral regions, by contrast, are much more informative about how much sex our ancestors had with archaic Homo species. Natural selection is blind to these regions, so their frequency in the gene pool drifts up and down by pure chance. Any introgressed sequences will be few in number, and the vast majority will at some point drop out of the gene pool altogether. Just a few, however, will win the genetic lottery and persist in modern humans. The more interbreeding occurred, the more introgressed neutral regions remain. Hammer's group has already found several neutral regions that look like they are introgressions. "It doesn't seem that it was a particularly rare event -- it looks like it's happening enough that neutral regions can introgress into the genome and persist in modern populations," says Hammer. 5/8

6 One example even tells a possible story of interbreeding between humans and an even more distant ancestor, Homo erectus. The pseudogene RRM2P4 -- a remnant of a now-defunct gene -- shows even deeper deep ancestry than PDHA1. RRM2P4 comes in two basic types that diverged 2 million years ago -- around the same time that Homo erectus first moved out of Africa into Asia. Crucially, one type is found almost exclusively in people of east Asian origin. According to Hammer and Garrigan, the most likely explanation for this deep ancestry and geographical distribution is that the pseudogene evolved in the Asian branch of Homo erectus and introgressed into Homo sapiens (Molecular Biology and Evolution, vol 22, p 189). That event is certainly not ruled out by the fossil record: recent finds suggest that Homo sapiens and Homo erectus coexisted in Asia for several thousand years. While most biologists accept that interbreeding was possible, introgression is not the only way to explain patterns in the genome that don't fit in with the single-origin view. Multiregionalism is one alternative. Another is that natural selection has acted on what we wrongly believed are neutral regions in the genome, distorting the frequency and distribution of genes across the globe. "We have a lot of different models," says Tishkoff at the University of Maryland. "The real challenge is trying to distinguish between them." Hammer is also wary of jumping to conclusions. "When we find a region of the genome that shows this pattern of introgression we really have to argue that the pattern didn't arise by some form of selection, which might also produce similar patterns." Even so, a broad consensus seems to be emerging about our ancestry, and it includes interbreeding as an important element. "There was a great genetic contribution from one African population, but the genetic material that existed in other localised archaic populations was not lost forever -- it was integrated into the modern human genome," says Garrigan. Trinkaus, who has long argued that humans picked up genes from other archaic humans, sees a similar picture. The extremes of single origin on the one hand and global multiregionalism on the other are "intellectually passé," he says. "The basic model is 'out of Africa' -- with admixture. The issue is how much, where, and when." As always in science, the answer to those questions lies in gathering more data. With the advent of $1000 genome sequencing, predicted to be a reality within five years, it will be possible to sequence vastly more genomes than are available today. Researchers can then seek a complete picture of the puzzling patterns of ancestry locked away in our genomes. Then, at last, we may know whether the Lagar Velho child was part of a hybrid population heading down an evolutionary dead end, or an ancient reminder of the Neanderthal in all of us. Wisdom of bones Dan Jones Dan Jones is a science writer based in Brighton, UK The Lagar Velho child unearthed in Portugal isn't the only skeleton that has been identified as a possible human-neanderthal hybrid. In the past few years Erik Trinkaus of Washington University in St Louis, Missouri, has amassed more fossil evidence that he says tells the same story. 6/8

7 In 2002, a team of cavers discovered a human jawbone in a cave called Pestera cu Oase ("cave with bones") in south-west Romania. Carbon dating put the remains at about 40,000 years old, which made it the earliest unambiguous modern human specimen found in Europe. Even a single bone can contain features characteristic of either Neanderthals or modern humans. According to Trinkaus, the Oase 1 jawbone has a mixture of both. Though less dramatically a hybrid than the Lagar Velho child, the find still suggests interbreeding. Further exploration of Pestera cu Oase has yielded even greater treasures. In January, Trinkaus and colleagues described a human skull which they called Oase 2 (Proceedings of the National Academy of Sciences, vol 104, p 1165). This seems to be the remains of an adolescent who also died about 40,000 years ago and, like the Oase 1 sample, has a mixture of modern and Neanderthal features (see below). Trinkaus has also reanalysed some 35,000-year-old human bones discovered in 1952 at another site in Romania, Pestera Muierii, and says that these too show a mosaic of features. To Trinkaus, these finds paint a fairly clear picture of the evolution of humans in Europe. "Early European humans are basically modern -- their anatomy is overwhelmingly like that of the ancestral African population -- but in individual specimens you find features that are absent from or have already been lost from the ancestral African group," says Trinkaus. "By far the easiest way to explain this is through interbreeding." This is not to suggest that the Lagar Velho boy or the Romanian specimens are the product of occasional, one-off meetings between Neanderthals and Cro-Magnons. Trinkaus suggests a more radical notion: the hybrids come from a population of humans that regularly interbred with Neanderthals. In other words, they are the result of generations of sex between Neanderthals and Cro-Magnons. Not everyone agrees with his argument. Human ancestry, like beauty, is in the eye of the beholder. For instance, Chris Stringer, a palaeontologist at the Natural History Museum in London, is not convinced that the Lagar Velho boy is evidence of hybridisation. "In many respects, including face and teeth, it's a modern human; the only place where it might look archaic is in the body proportions, but to me they overlap with those of other modern humans," he says. "I just don't see the Neanderthal influence that Erik does." Stringer believes more fossil evidence is required. "When we have a reasonable sample of early moderns dating from the same time period as the main sample of Neanderthals in Europe -- 40,000 to 70,000 years ago -- from regions such as western Asia or north Africa, then we will be able to see what their morphology was and will be able to better determine whether features have come from Neanderthal admixture." ~~~~~~~~ By Dan Jones 7/8

8 2007, New Scientist, Reed Business Information UK, Ltd., a division of Reed Elsevier, Inc. All Rights Reserved. Copyright of New Scientist is the property of Reed Business Information and its content may not be copied or ed to multiple sites or posted to a listserv without the copyright holder's express written permission. However, users may print, download, or articles for individual use. 8/8

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