Dawn-of-the-Dog

NEWSFEATURESDAWN OFTHE DOGAn unprecedented collaborationmay solve one of the greatest mysteriesof domesticationBy David Grimm, in Columbus, OhioAprehistoric dog is about to goto the dentist. Ardern Hulme-Beaman, a lanky 27-year-old Irishpostdoc, pulls on a white facemaskand lifts a small 5000-yearoldjawbone from a cardboardbox. He places a gloved handover one of the molars and gentlytugs from side to side untilit pops out. The jagged top of the tooth isyellowish white, but the roots are dirtybrown. Hulme-Beaman powers on a drill,and a circular blade screeches into a root.The scent of burning hair fills theair. “That’s a good sign,” he says. “Itmeans there’s DNA here.”Hulme-Beaman has spent thepast 6 months traveling the worldin search of ancient dog boneslike this one. He’s found plentyin this Ohio State University archaeologylaboratory. Amid boxes stacked high withNative American artifacts, rows of plasticcontainers filled with primate teeth, and ahodgepodge of microscopes, calipers, andresearch papers, a few shoe and cigar boxeshold the jigsaw pieces of a dozen canines:skulls, femurs, mandibles, and vertebrae.It’s all a bit of a jumble, which seems appropriatefor a field that’s a bit of a mess itself.Dogs were the very first thing humansdomesticated—before any plant, before anyother animal. Yet despite decades of study,researchers are still fighting over where andMORE ONLINEFor a video, quiz,and more, seehttp://scim.ag/k9science.when wolves became humans’ loyal companions.“It’s very competitive and contentious,”says Jean-Denis Vigne, a zooarchaeologist atthe National Museum of Natural History inParis, who notes that dogs could shed lighton human prehistory and the very nature ofdomestication. “It’s an animal so deeply andstrongly connected to our history that everyonewants to know.”And soon everyone just might. In an unprecedentedtruce brokered by two scientistsfrom outside the dog wars, the various factionshave started working together. Withthe help of Hulme-Beaman andothers, they’re sharing samples,analyzing thousands of bones,and trying to set aside years ofbad blood and bruised egos. If theeffort succeeds, the former competitorswill uncover the historyof man’s oldest friend—and solve one of thegreatest mysteries of domestication.CHARLES DARWIN fired the first shotin the dog wars. Writing in 1868 in TheVariation of Animals and Plants underDomestication, he wondered whether dogshad evolved from a single species or froman unusual mating, perhaps between awolf and a jackal. Decades of speculationfollowed, until in the late 1990s, geneticanalyses finally confirmed that dogs haddescended from gray wolves. (The twoshare 99.9% of their DNA.)Downloaded from www.sciencemag.orgon April 17, 2015274 17 APRIL 2015 • VOL 348 ISSUE 6232 sciencemag.org SCIENCEPublished by AAAS

Dogs have helped humans since prehistory. Here theyaccompany a caravan transporting salt in Tibet.But just when and where this transitionhappened was a mystery. In 1977, scientistsdiscovered a puppy buried in the arms ofa human under a 12,000-year-old home innorthern Israel, suggesting that dogs weredomesticated in the Middle East, shortlybefore people took up farming. But laterfinds—skulls recovered from Russian cavesand from ancient encampments in Germany—pushed canine origins back another 4000years, indicating that dogs accompaniedpeople in Eurasia while they were stillhunters and gatherers.Genetic investigations have only complicatedthe picture. A 1997 analysis of DNAfrom more than 300 modern dogs andwolves tallied genetic differences, aimingto use these as a measure of time since dogsbegan to diverge from their wolf ancestor.It concluded that dogs may have been domesticatedas early as 135,000 years ago.Later studies argued for a more recentorigin—less than 30,000 years ago—but theexact time and location remained unclear.“There were lots of books written, andthey all said something completely different,”says Peter Savolainen, a geneticist atthe Royal Institute of Technology in Stockholm.Savolainen had become interested inthe topic in the early 1990s as a master’sstudent in a government forensics lab,where he set up the world’s first canineDNA database to help police with two unsolvedmurders. Dog hair had been foundon the bodies, and by collecting geneticmaterial from 100 canines across the globe,he helped the officers determine the type ofdog the murderer owned.Savolainen knew that DNA had been usedto pinpoint Africa as the place where modernhumans emerged, and he wondered if asimilar approach could help him home in onthe birthplace of dogs. “Already in our smalldatabase, I saw a pattern,” he says. East Asianbreeds were more genetically diverse—a hallmarkof more ancient origins. As Savolainencontinued to build his database, the patternremained. In 2009, he published a geneticanalysis of more than 1500 dogs from aroundthe world, concluding that the animals hadlikely arisen in a region south of China’sYangtze River less than 16,300 years ago—atime when humans were transitioning fromhunting and gathering to rice farming. Theseearly canines, his team speculated, may havebeen raised for meat. “The data are very clearand distinct,” he says. “For me, the basicquestion is solved.”Not for Robert Wayne, an evolutionarybiologist at the University of California, LosAngeles. The elder statesman of canine ge-SCIENCE sciencemag.org17 APRIL 2015 • VOL 348 ISSUE 6232 275Published by AAAS

NEWS | FEATURESnetics, Wayne began working on dog DNAin the early 1980s, when genetic sequencingwas still in its infancy. Like Savolainen, he’sinterested in where dogs came from. But thetwo have come to very different conclusionsand have been sparring in papers and thepress for more than a decade.That’s largely because Wayne thinks lookingat modern DNA is a mistake. “We havethis image of dogs living in our homes andgoing on walks with us,” he says. “But that’snot the way it was in the past.” Dogs regularlyinterbred with wolves and caninesfrom other regions—especially in China, hesays, where traffic along major trade routeslikely brought in breeds from Europe, theMiddle East, and elsewhere in Asia. Anygenetic diversity in modern Asian dogs, hesays, may simply be a result of all of thesefar-flung animals mating. “It would belike concluding that humans arose in theUnited States because there’s so much geneticdiversity here.”Instead, Wayne focuses more on ancientDNA, hoping to peer back to a time whendog populations were relatively isolatedfrom one another. In 2013, he and his colleaguespublished the most extensive analysisof ancient dog and wolf genomes todate. Comparing the DNA of 18 dog- andwolflike bones from Eurasia and Americato that of modern dogs and wolves fromaround the world, the study found that theDNA of ancient dogs most closely matchedthat of European wolves, and the DNA oftoday’s dogs most closely matched that ofancient wolves.That led the group to conclude that dogsevolved from a now-extinct group of wolvesin Europe, somewhere between 19,000and 32,000 years ago. These early dogsmay have resembled Siberian huskies onsteroids—their hunting prowess and abilityto carry heavy loads a boon to ice agehumans as they pursued mammoths andother large game across a frigid continent.Savolainen pounced on the study, callingit “geographically biased” in a 2013 storyin The New York Times, because Wayne’sgroup hadn’t used any samples from SoutheastAsia. “It’s like studying the geographicalorigins of humans without including asingle sample from Africa,” he says. Wayneshot back, saying he hadn’t included ancientspecimens from China because therewere none—a fact, he said, that cast furtherdoubt on the view that dogs had originatedthere. “I think we’ve reached an impasse,”Wayne says. “We don’t interact much.”Greger Larson holds a wolf skull at the OxfordMuseum of Natural History (top). ArdernHulme-Beaman (bottom) examines an ancientdog jawbone (middle).PHOTOS: © JOHN CAIRNS (3); (PREVIOUS PAGE) © KAZUYOSHI NOMACHI/CORBIS276 17 APRIL 2015 • VOL 348 ISSUE 6232 sciencemag.org SCIENCEPublished by AAAS

PHOTO: © MARC MORITSCH/NATIONAL GEOGRAPHIC CREATIVE/CORBISGeneticists aren’t the only ones brawling.In 2009, paleontologist Mietje Germonpréreported finding an unusual skull in thearchives of her museum, the Royal BelgianInstitute of Natural Sciences in Brussels.Though the scientist who had originally unearthedthe skull from Goyet Cave in southernBelgium pegged it as a wolf cranium,Germonpré’s measurements indicated thatit belonged to a dog. Radiocarbon datingrevealed that the skull was 32,000 yearsold—so much older than other ancient dogremains known at the time that it couldhave finally stamped a time and place oncanine beginnings.Critics chomped, calling Germonpré’sanalysis “premature” and “misleading.”They said the specimen, like some otherancient putative dog skulls, could merelybe a strange-looking wolf. Germonpré respondedthat the creature may have beenan early dog that didn’t give rise to today’scanines—a primitive attempt at domesticationthat hit a dead end. “It’s a very combativefield,” she sighs. “More than any othersubject in prehistory.”ENTER GREGER LARSON and KeithDobney. The two had met in the early 1990sin Turkmenistan, where Dobney and a largegroup of other British archaeologists wereexcavating an early farming village. Larson—fresh out of college in California—showed upunannounced, wearing a baseball cap andloafers. The archaeologists, in their floppyhats and scruffy trousers, “thought he wasjust another preppy American,” Dobney says.Yet Larson quickly impressed the scientists,asking a volley of incisive questions abouttheir work. “It was a bit irritating, but hisenthusiasm was infectious,” Dobney says.Within a few days, Larson was shotgunningbeers with his new pals.The two began working together a fewyears later when Larson was a Ph.D. studentat the University of Oxford and Dobney wasback at the University of Aberdeen, both inthe United Kingdom. Both were interestedin the domestication of the pig—an animalthat, like the dog, had played a crucial rolein early human history but whose originswere murky. Their initial work, based onmodern DNA, suggested that humans hadindependently domesticated wild boar inseveral locations. But when they combinedancient DNA with a relatively new techniqueknown as geometric morphometrics—whichinvolves taking thousands of measurementsof bones to see how their shapes differ betweenindividuals—they discovered that along history of trading and interbreedinghad created the impression of numerousdomestication events when there were likelyonly one or two.How the wolf became the dog By David GrimmA gray wolf.Scientists who study canine origins seem to fight about everything: wheredogs arose, when this happened, and even the best way to find these answers.But there’s one thing most of them agree on: how dogs became domesticated.Still, it’s taken almost a century to get here, and the details are still emerging.In 1907, the English scientist Francis Galton suggested that dogs firstentered our lives when our ancestors nabbed some wolf pups, brought them backto camp, and raised them as pets. If you’ve ever seen a baby wolf, with its big eyesand oversized ears, the idea doesn’t seem so far-fetched—and, indeed, Galton’shypothesis reigned for decades. But scientists eventually realized that domesticationis a long, messy process that can take hundreds or even thousands of years.These early humans may have started with a cute pup, but they would have endedup with a wild animal.So what did happen? Most experts now think dogs domesticated themselves.Early humans left piles of discarded carcasses at the edges of their campsites—averitable feast, the thinking goes, for wolves that dared get close to people. Thosewolves survived longer and produced more pups—a process that, generation bygeneration, yielded ever-bolder animals, until finally a wolf was eating out of a person’shand. Once our ancestors realized the utility of these animals, they initiateda second, more active phase of domestication, breeding early canines to be betterhunters, herders, and guardians.A massive collaboration that’s trying to figure out where and when dogs emerged(see main story, p. 274) has found some intriguing insights into the second phase ofdog domestication. A comparison of thousands of ancient dog and wolf skeletons,for example, has revealed flattening of the dorsal tips of ancient dog vertebrae,suggesting that the animals hauled heavy packs on their backs. The team has alsospotted missing pairs of molars near the rear of the jaw in ancient dogs, which mayindicate that the animals wore some sort of bridle to pull carts. These services, inaddition to dogs’ hunting prowess, may have proved critical for human survival,potentially allowing modern humans to outcompete our Neandertal rivals and eveneventually settle down and become farmers.Now, a study on page 333 helps explains how man and dog took the next step tobecome best friends. Takefumi Kikusui, an animal behaviorist at Azabu Universityin Sagamihara, Japan, and his colleagues have found that when dogs and humansgaze into each other’s eyes, both experience a rise in oxytocin—a hormone that hasbeen linked to trust and maternal bonding. The same rise in oxytocin occurs whenhuman mothers and infants stare at each other, suggesting that early dogs mayhave hijacked this response to better bond with their new human family.The oxytocin study and the skeletal data from the new collaboration go beyondclarifying the origin of the family pet, says collaboration leader Greger Larson, anevolutionary biologist at the University of Oxford in the United Kingdom. “Themore that we know about the process of how dogs became associated with people,the more we learn about the origins of civilization.” ■SCIENCE sciencemag.orgPublished by AAAS17 APRIL 2015 • VOL 348 ISSUE 6232 277

A dog skull sits on a disk,as scientists prepare tophotograph it for geometricmorphometrics.“When all these dog papers started comingout, we got really frustrated,” says Larson,now an evolutionary biologist at Oxford. “Wefelt we had done more with pigs.” He thoughtthat Wayne hadn’t accurately distinguishedbetween ancient wolf and dog bones and thathis samples were too geographically limited.Yet he also faulted Savolainen for trying touse modern DNA as a windowinto the past. “It’s like a gianttomato soup with just onecolor,” he says. “You can’t goback and figure out what theingredients are.”Larson and Dobney wantedto take a lesson from theirpig work—analyzing as manysamples as possible from asmany places as possible andcombining ancient DNA analysiswith geometric morphometrics.But in order to dothis, they were going to haveto bring everyone together.Money proved a great motivator.Though dogs loomlarge in the public consciousness,they don’t tendto loosen the purse stringsof funding organizations.As a result, many scientistswork on them as only ahobby or side project, piggybackingon funding fromother grants. But Larson andDobney made a strong caseto European funding agenciesin 2012, arguing thatthe domestication of dogsset the stage for taming anentire host of plants and animals.“We said, without dogsyou don’t have any other domestication,”Larson says. “You don’t have civilization.”The approach worked. The duo secured$3 million and began calling people up.“We told them, ‘We’re going to do this. Wehave the finances. We want you on board,’ ”Larson says. His personality helped. “Everybodylikes him,” Dobney says. “People don’tWolf versus dogTraditionally, researchers used the traits below to distinguish wolves fromdogs, but geometric morphometrics may reveal new nuances.Dogs have a relativelyshorter snout.Canines are generallysmaller, finer in dogs.The wolf snout slopesdown gently, whereasthe dog snout has a kinkin front of the eyes.Wolf teeth tend to beless crowded.see him as a rival.” Larson also took ego outof the equation. “I told everyone, ‘I don’tgive a shit where I am as an author on thesepapers—I just want to get them out.’ ”By the end of 2013, Larson and Dobneyhad attracted 15 collaborators, includingWayne, Savolainen, and Germonpré. In a2-day conference in December, they hammeredout the details ofthe project. “You could feelthe tension in the room,”DogWolfDobney recalls. But Larsonsoothed the small crowd.“Everything is water underthe bridge,” he told them.“We all have a stake in this.”Savolainen was intriguedby the opportunity to delveinto new data sets. “There’salways more to learn,” hesays. And Wayne was excitedto analyze moresamples. “Greger won thetrust and confidence of alot of people,” he says. “That’sa real skill.” Now, they justhad to get their hands onthousands of bones.BACK AT OHIO STATE,Hulme-Beaman is drillinginto a second dog molar, butthis time he seems nervous.The tooth has a hairlinecrack, and he’s worried it willfracture or explode: preciousDNA lost in the dust, an irreplaceablemuseum specimendestroyed. But he gets lucky;the root saws clean off, andthe rest of the molar remainsintact. Hulme-Beaman plugsPHOTOS: (TOP TO BOTTOM) © JOHN CAIRNS; ARDERN HULME-BEAMAN, PHOTOGRAPHED AT THE SWEDISH MUSEUM OF NATURAL HISTORY (2)278 17 APRIL 2015 • VOL 348 ISSUE 6232 sciencemag.org SCIENCEPublished by AAAS

NEWS | FEATURESPHOTO: © THE UPPER GALILEE MUSEUM OF PREHISTORYthe tooth back into its mandibleand slots the root intoa tiny Ziploc bag, where itwill be shipped to the UnitedKingdom for genetic analysis.“That’s about as good asit can go,” he exhales.The postdoc has made11 trips as one of the dogcollaboration’s two mainsample hunters, travelingfrom his home base at theUniversity of Aberdeen toother universities, museums,and even private collections.“I’m on a plane ortrain every 2 to 3 weeks,”he says. He’s probed wolfskulls in Serbia, cradleddog bones in Sweden, andscoured the archives of theSmithsonian Institution inWashington, D.C. Most ofthe destinations come fromscanning the scientific literature,talking to experts,and putting up posters atprofessional and amateurarchaeology conferences.“There’s a huge amountthat’s hidden in desk drawers,”he says.Hulme-Beaman is at OhioState because of a callLarson received from PaulSciulli, a retired physicalanthropologist who heardabout the collaboration. Hetold Larson he had accessto a bunch of ancient NativeAmerican dogs, some ofwhich he had dug up himselfin unexpected places. “There are siteswhere you find nothing,” says Sciulli, whohas swung by to check on Hulme-Beaman’sprogress. “No houses, no signs of villagelife. Just graves. And it’s just people anddogs.” Most of the dogs were about the sizeof beagles, and some were buried with theirowners, one under a person’s arm. “Theseweren’t wild animals,” he says. “They werepart of the family.”Sciulli watches as Hulme-Beaman moveson to another specimen, gingerly removinga yellow-brown cranium the size of a pineapplefrom a plastic bag. He places the sampleon a record-size disk, beneath a cameraattached to a jointed mechanical arm. Thenhe slowly rotates the disk, snapping a pictureevery 2 seconds as the images appearon a nearby laptop. “We’re tricking thecomputer into thinking that we’re walkingaround the object,” he explains. By the timethe disk has done a 360, he has taken moreThe skeletons of a human and dog (upper left) discovered underneath a 12,000-year-oldhome in northern Israel are early evidence of the human-canine bond.than 200 shots, and a three-dimensionalrendering of the skull pops up on the screen,rotating to expose every nook and cranny—a carbon copy cranium Hulme-Beaman canbring anywhere.The computer can now do somethingno archaeologist can: perform geometricmorphometric analysis of the skull. Thethousands of measurements it will takewill go far beyond mere length and widthto determine actual shapes: the precise circletsof eye sockets, the jut and jag of everytooth. Ancient DNA, Hulme-Beaman says,can tell you where an animal came from,but only such morphometric data can showyou domestication in progress—the sharperangling of the snout, for example, that tookplace as wolves morphed into dogs.“For the first time, we’re going to be ableto look at some of these strange skulls likethe Goyet skull and figure out how strangethey really are,” he says. “Are they wolvesbecoming dogs, or are theyjust unusual wolves?” Combiningthe two approaches,he says, should allow thecollaboration to home in onjust where dogs came from—and when this happened.“Archaeology is storytelling,”Hulme-Beaman says.“I think we’re going to beable to tell a great story.”AT THE END OF THE DAY,Hulme-Beaman packs up hislaptop and samples and preparesfor his next trip, likelyto Istanbul. Sciulli suggestsa detour, mentioning a museumin Cleveland that has“hundreds of bones” from alocal site; he says he can putthe curator in touch. Hulme-Beaman looks tired, but hesmiles. “Sure,” he says, “giveme his number.”A continent away, Larsonand Dobney have continuedto make phone calls.Their collaboration hasnow swelled to 50 scientistsfrom around the world—experts on dogs, domestication,zooarchaeology, andgenetics. Larson estimatesthat the team has analyzedmore than 3000 wolf, dog,and mystery specimensso far, and he expects thegroup to submit its first paperthis summer. “I’ve beenreally encouraged by howeveryone has been gettingalong,” he says. “We have a lot more in commonthan we thought.”Larson feels confident that the work willsolve the mystery of dog domesticationonce and for all, though some experts aren’tso sure. Just throwing a lot of data at anenigma won’t necessarily unravel it, warnsRichard Meadow, the director of the zooarchaeologylaboratory at Harvard University’sPeabody Museum. “The more samplesyou get, the more complicated things get.”And Hulme-Beaman points out that even ifthere is an answer, it’s likely to disgruntlesome of the collaborators.Still, the formerly warring camps seemsanguine. “I’m willing to accept a differentresult,” Savolainen says. “If I’m wrong, it willbe a bit embarrassing,” he laughs, “but scienceis about trying to find the truth.” Wayneagrees. “Even if what we find contradicts myhypothesis, I’d be very happy,” he says. “I justwant an answer.” ■SCIENCE sciencemag.org17 APRIL 2015 • VOL 348 ISSUE 6232 279Published by AAAS