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Feature THE HIDDEN HISTORY OF ANCIENT PLAGUES A finding that Vikings carried smallpox virus shows how genetics is changing our knowledge of past diseases. By Laura Spinney he death date of smallpox is clear. caused by the bacterium Yersinia pestis5. Remains of a smallpox carrier buried in After killing more than 300 million Not all genetic studies have moved disease Öland, Sweden, between AD 800 and 1050. people in the twentieth century, it origins backwards in time, however: in 2014, a claimed its last victim in 1978; two German-led group reported that tuberculosis evidence of disease, spotting the telltale years later, on 8 May 1980, the World had been infecting humans for less than 6,000 signs of leprosy or syphilis, for instance, and Health Assembly declared that the years, not 12,000 as the consensus had been, cross-referencing with historical records. But variola virus, which causes small- let alone 70,000 years as had previously been many infections don’t leave visible marks on pox, had been eradicated. But the suggested6. bone. Other, indirect clues to the age of some Torigins of this devastating virus are obscure. These findings are shaking up researchers’ diseases have come from estimating the age Now, genetic evidence is starting to uncover understanding of how diseases have affected and geographical distribution of protective when smallpox first started attacking people. human populations throughout history, says mutations in humans: people whose red blood Humans as far back as ad 600 carried Ann Carmichael, a plague historian at Indiana cells lack the ‘Duffy antigens’, for example, variola, an international research team University in Bloomington. The DNA evidence enjoy some protection against the malaria reported this week1 after years of fishing for suggests that diseases such as plague and parasite Plasmodium vivax. viral DNA in ancient human remains. The analy- hepatitis B are associated with major prehis- Researchers have been able to fish out sis also implies that the virus was circulating in toric migrations — something that seems now fragments of pathogen DNA from remains humans even earlier: at least 1,700 years back, to be true of variola too. Whether migrations since the 1990s. And in the past decade, in the turbulent period around the fall of the brought the diseases to new areas or the emer- next-generation DNA sequencers that can read Western Roman Empire, when many peoples gence of disease triggered people to move is myriad short snippets — useful for sequencing were migrating across Eurasia. a question that archaeologists, historians and DNA damaged after hundreds or thousands of The research pushes DNA evidence of geneticists hope to be able to answer. years — have helped researchers reconstruct smallpox back by a millennium. In 2016, entire genomes of ancient pathogens. In 2011, researchers had dated it to the seven- “High-definition timing scientists published the first such genome7, of teenth century, using DNA extracted from a Y. pestis, gathered from four skeletons in a Lon- Lithuanian mummy2. “We’ve shown that 1,000 will be critical to rewriting don graveyard where thousands of Black Death years earlier, during the Viking Age, variola human history.” victims were buried in the fourteenth century. was already quite widespread in Europe,” says It is now routine to screen ancient human Martin Sikora, an evolutionary geneticist at remains for known pathogens, says Eske Will- the University of Copenhagen and a member The DNA evidence has also provided erslev, an evolutionary geneticist at the Uni- of the team. insights into the virulence of ancient versity of Cambridge, UK, who worked on the Smallpox is only the latest example of a smallpox: the latest work suggests that the smallpox study. This began as an offshoot of serious infectious disease whose history has Vikings, for instance, carried an extinct vari- a project8 to chart the Viking diaspora of the been suddenly and substantially rewritten by ola lineage quite different from the modern late first millennium ad, but grew into a much ancient-DNA analysis in the past decade. Earlier strain. Integrating the genetics with history larger analysis. Researchers screened DNA this year, a study3 reported that the measles and archaeology is the work that lies ahead, collected from 1,867 individuals who lived in virus — thought to have emerged in humans says archaeologist Søren Sindbæk of Aarhus Eurasia and the Americas between 32,000 and around the ninth century — might have jumped University in Denmark. “We can begin to nail 150 years ago. They found stretches of DNA to people in the first millennium bc, which is these events down to the human scale,” he says. that resembled modern variola strains in 26 when its sequence seems to have diverged “Going forward, high-definition timing will be of them; for 13, they were able to go back to from the related (and now-eradicated) critical to rewriting human history.” the original remains and extract more variola rinderpest virus, which infected cattle. In DNA through targeted capture, a technique 2018, Sikora’s team showed that hepatitis B had Ancient pathogen genomes that uses laboratory-synthesized DNA to been infecting humans since the Bronze Age, Before the ancient-DNA revolution, pick out similar strands from bones or teeth. 5,000 years ago4; in 2015, the team reported a researchers had to rely on examining skeletons (Researchers have homed in on the petrous similarly early origin for the plague, which is — or, more rarely, mummies — for visible bone — a part of the skull close to the ear — as BOARD HERITAGE NATL SWEDISH 30 | Nature | Vol 584 | 6 August 2020 ©2020 Spri nger Nature Li mited. All rights reserved. ©2020 Spri nger Nature Li mited. All rights reserved. Nature | Vol 584 | 6 August 2020 | 31 ©2020 Spri nger Nature Li mited. All rights reserved. ©2020 Spri nger Nature Li mited. All rights reserved. Feature ANCIENT SMALLPOX discovery of Y. pestis in the preserved teeth of The discovery of the variola virus, which causes smallpox, in Viking-era remains Yamnaya herders who came to Europe from shows that the disease has been present in humans for at least 1,700 years. the eastern European steppe, for example, has 1000 BC 500 AD 1 500 1000 1500 2000 Year given rise to the theory that these invaders accel- erated the decline of Neolithic farming socie- Modern* ties after 3500 bc by spreading plague among variola strains them. But this is still a contested idea because *Smallpox there is archaeological evidence that a decline eliminated in 1980. was already under way 1,000 years before the Yamnaya arrived, says Detlef Gronenborn, an Viking-age archaeologist at the Leibniz Research Institute variola strains for Archaeology in Mainz, Germany. ? Modern strains But because only around 200 complete diversified around ancient-pathogen genomes have been 430 years ago. sequenced9 — and only a few for each pathogen Camelpox — conclusions that can be drawn from phylo- Taterapox (gerbils) genetic analysis are limited for now. Even in the current pandemic, with tens of thousands of Unknown animal virus jumps into Variola found in Viking-era remains might humans, giving rise to human have shared a common ancestor with SARS-CoV-2 genomes analysed, researchers variola; timeline uncertain. modern strains around 1,700 years ago. have sometimes drawn erroneous conclu- 1 JONES/REF. & T. M.SIKORA MÜHLEMANN, B. SOURCE: sions about the path the virus took during its a good source of ancient DNA, because it is the widely before 3,000–4,000 years ago. spread10. The further researchers go back in densest mammalian bone and so preserves Other researchers have surmised that time and the sparser the samples, Poinar says, human DNA well. But pathogens are more variola was infecting humans well before the greater the risk of over-interpretation. likely to show up in the teeth, because more 1,700 years ago. Historical records suggest Researchers say that investigations into the blood flows through them, says Willerslev.) that a smallpox-like disease has been with us evolutionary history of viruses might also be Eleven of these individuals dated from for more than 3,000 years, and might even helpful in protecting people in the future. “It’s around ad 600 to 1050, overlapping the have killed the young pharaoh Rameses V in very hard to predict where virus evolution is Viking Age, and they hailed from present-day the twelfth century bc — although nobody going to go,” says virologist Lasse Vinner of the Scandinavia, Russia and the United Kingdom. can be certain that he had smallpox or that, if University of Copenhagen, another author on One was unearthed from a mass grave in he did, the disease killed him. The latest DNA the paper, “but knowing where it has been, we Oxford, UK, and is thought to have died in the St evidence doesn’t shed any light on that idea, get a better idea of the possibilities of variation.” Brice’s Day Massacre of 1002, when the English but an Egyptian project to analyse the DNA of Andrea McCollum, an epidemiologist at the king Ethelred the Unready ordered the exter- royal mummies is scheduled to report in 2022. Centers for Disease Control and Prevention in mination of people identified as Danes. Four Scientists not involved in the variola study Atlanta, Georgia, who has studied smallpox, Viking-era individuals provided enough viral are impressed by the work. “This new paper says that such a family tree could be informative DNA for researchers to reconstruct near-com- is showing that there were lineages that about the protection that remaining stocks of plete variola genomes, which they compared we were completely ignorant about,” says smallpox vaccine would afford against related with modern variola sequences.

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