Out Of Southern East Asia: The Natural History Of Domestic .

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ORIGINAL ARTICLECell Research (2016) 26:21-33.www.nature.com/crOut of southern East Asia: the natural history of domesticdogs across the worldGuo-Dong Wang1, *, Weiwei Zhai2, *, He-Chuan Yang1, 2, 3, *, Lu Wang4, *, Li Zhong4, Yan-Hu Liu4, Ruo-Xi Fan4,Ting-Ting Yin1, 5, 6, Chun-Ling Zhu1, Andrei D Poyarkov7, David M Irwin8, Marjo K Hytönen9, Hannes Lohi9,Chung-I Wu10, Peter Savolainen11, Ya-Ping Zhang1, 41State Key Laboratory of Genetic Resources and Evolution, and Yunnan Laboratory of Molecular Biology of Domestic Animals,Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming 650223, China; 2Human Genetics, Genome Institute of Singapore, A*STAR, 60 Biopolis Street, Genome #02-01, Singapore 138672, Singapore; 3Department of Molecular and Cell Biology,School of Life Sciences, University of Science and Technology of China, Hefei 230026, China; 4Laboratory for Conservation andUtilization of Bio-resource & Key Laboratory for Microbial Resources of the Ministry of Education, Yunnan University, Kunming650091, China; 5University of Chinese Academy of Sciences, Beijing 100049, China; 6Kunming College of Life Science, Universityof Chinese Academy of Sciences, Kunming 650223, China; 7Severtsov Institute of Ecology and Evolution, Russian Academy ofScience, 33 Leninskiy Prospect, Moscow 119071, Russia; 8Laboratory Medicine & Pathobiology, University of Toronto, 1 King’sCollege Circle, Rm 6211, Toronto, ON, Canada M5S 1A8; 9Research Programs Unit, Molecular Neurology and Department of Veterinary Biosciences, University of Helsinki and Folkhälsan Research Center, Helsinki, Finland; 10Department of Ecology and Evolution, University of Chicago, 5801 S Ellis Ave, Chicago, IL 60637, USA; 11Department of Gene Technology, KTH-Royal Instituteof Technology, Science for Life Laboratory, Tomtebodavägen 23A, 17165 Solna, SwedenThe origin and evolution of the domestic dog remains a controversial question for the scientific community, withbasic aspects such as the place and date of origin, and the number of times dogs were domesticated, open to dispute.Using whole genome sequences from a total of 58 canids (12 gray wolves, 27 primitive dogs from Asia and Africa, anda collection of 19 diverse breeds from across the world), we find that dogs from southern East Asia have significantlyhigher genetic diversity compared to other populations, and are the most basal group relating to gray wolves, indicating an ancient origin of domestic dogs in southern East Asia 33 000 years ago. Around 15 000 years ago, a subsetof ancestral dogs started migrating to the Middle East, Africa and Europe, arriving in Europe at about 10 000 yearsago. One of the out of Asia lineages also migrated back to the east, creating a series of admixed populations with theendemic Asian lineages in northern China before migrating to the New World. For the first time, our study unravelsan extraordinary journey that the domestic dog has traveled on earth.Keywords: dog domestication; demography; Chinese indigenous dog; gene flow; artificial selectionCell Research (2016) 26:21-33. doi:10.1038/cr.2015.147; published online 15 December 2015IntroductionThe domestic dog (Canis lupus familiaris), one of ourclosest companions in the animal kingdom, has followedus to every continent of the world. As a single species,*These four authors contributed equally to this work.Correspondence: Ya-Ping Zhanga, Peter SavolainenbaE-mail: [email protected]: [email protected] 2 June 2015; revised 9 September 2015; accepted 10 October2015; published online 15 December 2015the domestic dog embodies one of the largest collectionsof phenotypic diversity for any species living on earth [1].Due to their cognitive and behavioral abilities, domesticdogs have been selected to fulfill a wide variety of tasksincluding hunting, herding and companionship. The genetic and historical basis of these phenotypic changes hasintrigued the scientific community, including Darwin [2].The history of dog domestication is often depictedas a two-stage process where primitive dogs were firstdomesticated from their wild ancestors, the gray wolves,and in the second stage, the primitive forms were further selected to form many dog breeds with specializednpg

npg Out of southern East Asia: the history of domestic dogs22abilities and morphology [3-5]. Despite many effortsstudying dog evolution, several basic aspects about theorigin and evolution of the domestic dog are still in dispute. For example, several different geographical regionshave been proposed as the birthplace of domestic dogs,and the date of divergence between wolves and dogs hasbeen estimated between 32 000 years ago and 10 000years ago [6-10], with relatively weak gene flows foundbetween these two groups since their divergence [4, 6, 7,9]. The exact history of dog domestication thus remainsto be fully resolved [11].The first comprehensive genetic investigations of thegeographical origin of dogs were based on global intraspecific studies of maternally transmitted DNA (mtDNA)in contemporary dogs, which gave a strong indicationthat dogs originated in the southern part of East Asia[7, 12]. However, several subsequent studies based ondiverse genetic markers have given discrepant answers.For example, using mtDNA from ancient dog samples,Thalmann et al. have suggested Europe as the place oforigin [13]. Likewise, using genome-wide genotyping ofmodern dogs, vonHoldt et al. found high haplotype sharing between Middle Eastern wolves and dogs, proposingthe Middle East as the major source of dog diversity [14].Although the datasets and approaches are different inthese studies, a common drawback of these single nucleotide polymorphism (SNP) array- and ancient DNAbased studies is a lack of samples from southern EastAsia, thus precluding evaluation of the possible scenariothat domestic dogs actually originated in this region. Inaddition, the use of a single locus, especially mtDNA,can skew the conclusion as it is more malleable by stochastic and/or selective forces [7, 12, 13]. Thus, the history of dog domestication remains enigmatic and highlycontroversial [11].Whole genome sequencing provides a powerful holistic approach to understanding the evolutionary history ofa species, and is sufficiently robust in mitigating problems such as SNP ascertainment bias or stochastic effectsacting on a single marker, which have influenced earlierstudies [15]. In this work, we collected the genome sequences of 58 canids from across the world, includingsamples from southern and northern parts of East Asia,Africa, Europe, the Middle East, Siberia and the Americas. Population genetic analysis reveals an ancient originfor the domestic dog in southern East Asia about 33 000years ago. After evolving for several thousand years inEast Asia, a subgroup of dogs radiated out of southernEast Asia about 15 000 years ago to the Middle East, Africa as well as Europe. One of these out of Asia lineagesthen migrated back to northern China and made a seriesof admixtures with endemic East Asian lineages, beforetraveling to the Americas. Our study, for the first time,reveals the extraordinary journey that the domestic doghas traveled on this planet during the past 33 000 years.ResultsSample collection and whole genome sequencing58 canids from around the world were gathered forthis study. This collection includes 12 gray wolves fromacross the Eurasian continent, 11 indigenous dogs fromsouthern East Asia, 12 indigenous dogs from northernEast Asia, 4 village dogs from Africa (Nigeria) and a setof 19 diverse dog breeds distributed across the Old Worldand the Americas.Chinese indigenous dogs are dogs living in the countryside of China [16] (Supplementary information, DataS1 and Figure S1) and were sampled across the geographic range of rural China, including many remoteregions in Yunnan and Guizhou in southern China (Supplementary information, Table S1). The breeds includedogs from Central Asia (Afghan Hound) and North Africa (Sloughi), Europe (eight different breeds), the Arcticand Siberia (Greenland dog, Alaska Malamute, Samoyed, Siberian Husky, and East Siberian Laika), the NewWorld (Chihuahua, Mexican and Peruvian naked dog) aswell as the Tibetan Plateau (Tibetan Mastiff). These dogswere chosen to cover as many major geographic regionsas possible (Figure 1A and Supplementary information,Table S1).After DNA extraction, individual genomes were sequenced to an average of 15 coverage (Supplementaryinformation, Table S1). Of the 58 individuals, 4 graywolves and 6 dogs have been sequenced in a previousstudy [10]. DNA sequence analysis was done using theGenome Analysis Toolkit [17]. After stringent filtering,we identified 20 353 184 SNPs and 3 856 246 smallindels (Figure 1B), most of which are shared betweengroups. For example, 40.3% of the SNPs are shared between wolves, indigenous dogs and dog breeds, reflecting their recent divergence (Figure 1B). Using Sangersequencing, we verified that the sequencing strategy washighly sensitive (false negative rate around 10%) and theamount of false positives was less than 5% (Supplementary information, Data S2 and Figure S2).Genetic diversity and population structureComparison of the two haploid genomes within eachindividual yields the genetic diversity θ (4 Nμ) for the58 individuals. As shown in Figure 1C, genetic diversityshows a decreasing trend from wolves to Chinese indigenous dogs (preserving 78% of the wolf heterozygosity)and subsequently to dog breeds (66% of the wolf heteroCell Research Vol 26 No 1 January 2016

Guo-Dong Wang et al. npg23Figure 1 Population structure and genetic diversity of 58 canids. (A) Geographic locations of the 58 canids sequenced in thisstudy. (B) Amount of of SNPs and small indels called in this study. (C) Genetic diversity for the 58 canids. AF, African villagedogs; BEM, Belgian Malinois; CHI, Chihuahua; FIL, Finnish Lapphund; GAL, Galgo; GNE, Gray Norwegian Elkhound; GSD,German Shepherd Dog; JAM, Jamthund; LAH, Lapponian Herder; MEN, Mexican naked (hairless); PEN, Peruvian naked(hairless); SWL, Swedish Lapphund; AFG, Afghan Hound; SLO, Sloughi; SAM, Samoyed; ESL, East Siberian Laika; SIH,Siberian Husky; ALM, Alaska Malamute; GRD, Greenland dogs; TIM, Tibetian Mastiff. (D) Structure analysis of the 58 canids.(E) Genetic diversity of the different groups. AF, African village dogs; EB, European breeds; SI, southern Chinese indigenousdogs; W, wolves. (F) Linkage disequilibrium patterns for the different groups. (G) Principle component analysis of the 58 canids. Inset is for all individuals and the large panel is for dogs only. (H) Principle component plot for a large collection of canids together with our data. (I) A clock-like tree (UPGMA) for all the 58 individuals [56].www.cell-research.com Cell Research

npg Out of southern East Asia: the history of domestic dogs24zygosity), with the African village dogs having a geneticdiversity comparable to many dog breeds (69% of thewolf heterozygosity). Among the dog breeds, the levelsof variation in genetic diversity are quite dramatic. Forexample, the East Asian breed Tibetan Mastiff and EastSiberian Laika show levels of diversity comparable tothe Chinese indigenous dogs, but many of the Europeandog breeds have considerably reduced genetic diversity.Such dramatic differences in genetic diversity can beinfluenced both by ancient and recent history of inbreeding.To explore the genetic relationships among these individuals, we performed a structure analysis using anexpectation maximization (EM) algorithm to cluster theindividuals into different numbers of groupings [18].When partitioning the individuals into two groups, thealgorithm separates the dogs from the wolves, with verylimited admixture observed (Figure 1D). Further dividingthe individuals into three subsets split the dogs into twoclusters, with indigenous dogs from southern East Asiarepresenting one subset and the other subset consisting ofdog breeds from Europe and South/Central America andthe African village dogs. Indigenous dogs from northernChina and dog breeds from the Arctic and Central Asia,the Middle East and North Africa show a mixture of thesecomponents with varying proportions. This observationimplies that there are two divergent groups of dogs: oneis East Asian component and the other, non-East Asiancomponent. It is important to emphasize that individualswith mixed constituents identified in the structure analysis are not always due to true admixture events, sincepopulations of intermediate genotypes between these twogroups tend to display mixed components (e.g., originated shortly after the split of two clades, Supplementaryinformation, Data S3 and Figure S3). Further partitioninginto four and five groups leads to the separation of theAfrican village dogs and the breed dogs from the easternArctic regions (i.e., Siberian Husky, Alaska Malamuteand the Greenland dog).Genetic diversity among individuals (Figure 1C) maybe heavily influenced by ancient as well as recent history, e.g., breeding programs during the last few thousandyears or the past few hundred years. However, combinedinformation from multiple breeds may reveal informationabout the ancestral populations that gave rise to them,since each breed has experienced separate breeding history. We therefore calculated the genetic diversity (θπ) forthe “pure groups” informed by the structure analysis (K 4, Figure 1D). As shown in Figure 1E, dog breeds, mostof which of European origin, carry lower diversity thanthe Chinese indigenous dogs as a group, but have highergenetic diversity than the African indigenous dogs. Thissuggests that the ancestral population that gave rise to theEuropean breeds was larger than the ancestral populationof the African indigenous dogs. Linkage disequilibriumpatterns also show similar trends (Figure 1F).Principle component and phylogenetic analysisWhen projecting the genotypes into a two-dimensional space using a principle component analysis (PCA)[19], all dogs cluster together tightly compared with thedistribution seen for wolves (Figure 1G, inset). Wheninspecting the distribution among dogs, we find that dogsspread along three major geographic axes: southern EastAsia, Europe and Africa. The northern Chinese indigenous dogs and dog breeds from the Middle East/Arcticregions/Tibet fall between these three extremes (Figure1G). The observed pattern reflects the overall geographiclocations of these groups following a clear East-Westgradient, which matches quite well the observation fromour structure analysis.Combining our dataset with data from a previous SNParray study, which included a larger number of samples[20], we found that the southern Chinese indigenous dogstogether with several East Asian dogs (e.g., Chow Chow,Akita, Chinese Shar-Pei) are closest to wolves (Figure1H). When the phylogenetic relationships among our 58samples are inspected, East Asian dogs spread over bothsides of the deepest node connecting all dogs, while dogsfrom other continental areas coalesce into a subclade andthen join with East Asian dogs. Thus, East Asian dogs arethe most basal lineages connecting to gray wolves (Figure 1I). It is worth pointing out that the genomes of dogsfrom Oceania (dingoes and New Guinea singing dogs),although being closer to wolves in the PCA plot (Figure1H), bear strong signals of admixture with gray wolves[6], which likely reflects their past history of admixture,before they migrated to Australia and New Guinea (Supplementary information, Data S4 and Figure S4).Admixture analysisUsing the joint allele frequencies among all populations in our study, we infer the split and admixture history among groups of populations using TreeMix [21]. Ifmigration tracks are not allowed, then the relationshipsinferred from the TreeMix analysis (Figure 2A) directlyreflect the patterns observed in our previous analysesincluding the structure (Figure 1D), the phylogenetic(Figure 1I) and the principal component analyses (Figure1G). Thus, following the divergence between contemporary wolves and domestic dogs, the first partition withindogs is between the southern Chinese indigenous groupand all other dogs. This is then followed by branchingof the other dogs, largely matching the geographical disCell Research Vol 26 No 1 January 2016

Guo-Dong Wang et al. npg25tance from southern East Asia: first, dogs from CentralAsia, northern China, and eastern Arctic, followed bydogs in Africa, the Middle East, and western Arctic, andthe final group including all dog breeds in Europe andSouth/Central America.If migration tracks are allowed in TreeMix, there isstrong statistical support for migrations among a fewgroups: (1) northern Chinese indigenous dogs showstrong admixture from European dogs (Figure 2A andSupplementary information, Data S5, Figure S5, TablesS2 and S3); (2) gene flow from wolves to the African/Middle Eastern dogs (Supplementary information, FigureS5); (3) migratory tracks from the southern Chinese dogsto the eastern Arctic group (i.e., Siberian Husky, AlaskaMalamute and the Greenland dog; Supplementary information, Figure S5). When all possible migration eventsin the history of these samples are examined using theF3/F4 test [22], there is again a strong statistical supportfor all the migration events listed above (Supplementaryinformation, Data S5).Long-term evolutionary trajectories for wolves and dogsUsing the divergence between the two haploid genomes within individuals, the pairwise sequentiallyMarkovian coalescent (PSMC) model provides a methodfor investigating the long-term trajectories in population sizes [23]. To translate demographic history intoreal-time units, estimation of an accurate mutation rateis very important. Previously, several different mutationrates were used, but they were generally not carefullycalibrated (Supplementary information, Data S6) [24].Using multiple outgroup species to the dog (e.g., horseand cat), our estimate of the mutation rate for the lineage leading to the domestic dog is 2.2 10 9 per siteper year (Supplementary information, Data S6 and TableS4), a rate similar to those from several earlier studies[25, 26]. Using this mutation rate, we estimate dates forthe population history of dogs and wolves. As shown inFigure 2B, a decrease in the size of the ancestral wolfpopulation started to occur 2 million years ago, reachinga saddle point about 3-400 000 years ago. The ancestralpopulation then increased in size, peaking at around200 000 years ago. After a subsequent small decline inpopulation size, wolves and dogs started to diverge fromeach other between 20 000 and 100 000 years ago (seenext section for a more precise dating). Although all domestic dogs drastically decreased in population size afterthe population split, the wolf population experienced aslight growth, possibly as a consequence of the megafauna extinctions (i.e., late Quaternary extinction) [27] thatprovided gray wolves with better food resources due toreduced competition from other predators.www.cell-research.com Cell ResearchTime of divergence between contemporary wolves anddogsTreemix and phylogenetic analyses identified southernChinese indigenous dogs as the most basal populationcompared to wolves, from which all other dog populations diverged. We therefore used joint allele frequenciesbetween the 12 gray wolves and the 11 southern Chineseindigenous dogs, to infer the demographic history forthese two populations with the dadi package [28]. Similarto the result from the PSMC analysis, the wolf population experienced a very mild population growth (1.26-foldincrease) that started around 290 000 years ago (Figure2C). The time of divergence for the wolf and dog populations is inferred to be around 33 000 years ago, wherethe domestic dog lineage expanded from a population of4 600 individuals to about 17 500.In addition to gauging changes in population size, statistical methods can also estimate the rates of exchangeof mi

across the Eurasian continent, 11 indigenous dogs from southern East Asia, 12 indigenous dogs from northern East Asia, 4 village dogs from Africa (Nigeria) and a set of 19 diverse dog breeds distributed across the Old World and the Americas. Chinese indigenous dogs are dogs living in the coun-tryside of China [16] (Supplementary information, Data

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