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The evolutionary history

of dogs in the Americas

Máire Ní Leathlobhair

*, Angela R. Perri

2,3

*, Evan K. Irving-Pease

*, Kelsey E. Witt

Anna Linderholm

4,6

*, James Haile

4,7

, Ophelie Lebrasseur

, Carly Ameen

Jeffrey Blick

†, Adam R. Boyko

, Selina Brace

, Yahaira Nunes Cortes

Susan J. Crockford

, Alison Devault

, Evangelos A. Dimopoulos

, Morley Eldridge

Jacob Enk

, Shyam Gopalakrishnan

, Kevin Gori

, Vaughan Grimes

, Eric Guiry

Anders J. Hansen

7,18

, Ardern Hulme-Beaman

4,8

, John Johnson

, Andrew Kitchen

Aleksei K. Kasparov

, Young-Mi Kwon

, Pavel A. Nikolskiy

21,22

, Carlos Peraza Lope

Aurélie Manin

24,25

, Terrance Martin

, Michael Meyer

, Kelsey Noack Myers

Mark Omura

, Jean-Marie Rouillard

14,30

, Elena Y. Pavlova

21,31

, Paul Sciulli

Mikkel-Holger S. Sinding

7,18,33

, Andrea Strakova

, Varvara V. Ivanova

Christopher Widga

, Eske Willerslev

, Vladimir V. Pitulko

, Ian Barnes

M. Thomas P. Gilbert

7,36

, Keith M. Dobney

8,37

, Ripan S. Malhi

38,39

Elizabeth P. Murchison

‡§, Greger Larson

‡§, Laurent A. F. Frantz

4,40

‡§

Dogs wer e present in the Americas befor e the arrival of European colonists, but the origin and

fate of these precontact dogs are largely unknown. We sequenced 71 mitochondrial and

7 nuclear genomes from ancient North American and Siberian dogs from time frames spanning

~9000 years. Our analysis indicates that American dogs were not derived from North

American wolves. Instead, American dogs form a monophyletic lineage that likely originated

in Siberia and dispersed into the Americas alongside people. After the arrival of Europeans,

native American dogs almost completely disappeared, leaving a minimal genetic legacy in

modern dog populations. The closest detectable extant lineage to pr econtact American dogs

is the canine transmissible vener eal tumor, a contagious cancer clone derived from an individual

dog that lived up to 8000 years ago.

he histor y of the global dispersal of dogs

continues to be contentious (1). In North

America, the earliest confirmed dog re-

mains (from Koster, IL) have been radio-

carbon dated to ~9900 calibrated years

before the present (2, 3), ~4500 years after the

earliest unambiguous evidence of humans arriv-

ing in the Americas (4). Although these early

dogs were most likely not domesticated in situ

(5), the timing of their arrival and their geo-

graphic origins are unknown. Studies of the

control region of mitocho ndrial DNA have sug-

gested that the precontact American dog pop-

ulation was largely replaced following the arrival

of European dogs after colonization and the in-

troduction of Eurasian Arctic dogs (e.g., Siberian

huskies) during the Alaskan gold rush (5–7). It

remains possible, however, that some modern

American dogs retain a degree of ancestry from

the precontact population (8, 9).

We sequenced complete mitochondrial ge-

nomes (mitogenomes) from 71 archaeological

dog remains collected in North America and

Siberia (Fig. 1A and table S1) and analyzed these

with 145 mitogenomes derived from a global data-

set of modern and ancient canids (3). A phylo-

genetic tree constructed from the mitogenomes

indicated that all sampled precontact dog s

(PCDs) (from time frames spanning ~9000 years)

formed a monophyletic group within dog haplo-

groupA(Fig.1Bandfigs.S3andS6).This

analysis indicated that the mitochondrial lineage

most closely related to the PCD clade is that of

the ~9000-year-old population of dogs from

Zhokhov Island in Eastern Siberia (3) (Fig. 1B

and figs. S3 and S6). In addition, molecular clock

analyses suggest that all PCDs share a common

ancestor that lived ~14,600 years ago [95% highest

posterior density (HPD), 16,484 to 12,965 years

ago] (Fig. 1B and fig. S6), which had diverged

from an ancestor shared with the Zhokhov Island

dogs ~1000 years earlier (95% HPD, 17,646 to

13,739 years ago) (Fig. 1B and f ig. S6). These

time frames are broadly coincident with early

migrations into the Americas (10–12).

To further investigate the evolutionary history

of PCDs, we generated low-coverage (~0.005 to

2.0×) nuclear genome sequences from seven

PCDs sampled in six locations in North America

from time frames spanning ~9000 years (table

S1). We analyzed these nuclear data alongside

publicly available datasets including 45 modern

canid whole genomes sampled from Eurasia

and the Americas (table S2) (13–16). A neighbor-

joining tree constructed by using single-nucleotide

polymorphisms (SNPs) revealed that, like the mito-

genome phylogeny, PCDs clustered in a distinct

monophyletic lineage that is more closely related

to dogs than to either Euras ian or North American

wolves (Fig. 1C). Furthermore, our nuclear genome

analysis indicated that the closest-related sister

clade to PCDs consists of modern Arctic dogs

from the Americas (including Alaskan malamutes,

Greenland dogs, and Alaskan huskies) and Eurasia

(Siberian huskies) (Fig. 1C). Treemix (3)(Fig.1D),

outgroup f3 statistics (fig. S13), and D statistics

(figs. S14 and S15) also supported this phylo-

genetic structure. Combined, our mitochondrial

and nuclear results indicate that PCDs were not

domesticated in situ from North American wolves

but were instead introduced by people into the

Americas via Beringia from a population related

to modern Arctic dogs.

Studies of nuclear genome data have identified

two modern clades of global dogs: an East Asian

clade (including dingoes) and a Western Eurasian

clade (including European, Indian, and African

dogs) (9, 14, 16). These analyses placed modern

Arctic dogs with either Western Eurasian (16, 17)

or East Asian (9, 14

) dogs. Our analyses of nuclear

genome

data revealed a close relationship be-

tween Arctic dogs and PCDs, which together form

RESEARCH

Ní Leathlobhair et al., Science 361,81–85 (2018) 6 July 2018 1of5

Transmissible Cancer Group, Department of Veterinary Medicine, University of Cambridge, Cambridge, UK.

Department of Archaeology, Durham University, Durham, UK.

Department of Human Evolution,

Max Planck Institute for Evolutionary Anthropology, Leipzig, Germany .

The Palaeogenomics and Bio-Archaeology Research Network, Research Laboratory for Archaeology and History of Art, University of

Oxford, Oxford, UK.

School of Integrative Biology, University of Illinois at Urbana-Champaign, Urbana-Champaign, IL, USA.

Department of Anthropology, Texas A&M University, College Station, TX, USA.

Centre for GeoGenetics, Natural History Museum of Denmark, University of Copenhagen, Copenhagen, Denmark.

Department of Archaeology, Classics and Egyptology, University of Liverpool, Liverpool,

UK.

Department of Government and Sociology, Georgia College and State University, Milledgeville, GA, USA.

Department of Biomedical Sciences, Cornell University, Ithaca, NY, USA.

Department of

Earth Sciences, Natural History Museum, London, UK.

Department of Anthropology, University at Albany–SUNY, Albany, NY, USA.

Pacific Identifications, Victoria, Canada.

Arbor Biosciences, Ann Arbor,

MI, USA.

Millennia Research, Victoria, Canada.

Department of Archaeology , Memorial University , Queen’s College, St. John’s, Canada.

Department of Anthropology, University of British Columbia,

Vancouver, Canada.

The Qimmeq Project, University of Greenland, Nuussuaq, Greenland.

Department of Anthropology, Santa Barbara Museum of Natural History, Santa Barbara, CA, USA.

Department

of Anthropology, University of Iowa, Iowa City, IA, USA.

Institute for the History of Material Culture, Russian Academy of Sciences, St. Petersburg, Russia.

Geological Institute, Russian Academy of

Sciences, Moscow, Russia.

Centro INAH Yucatán, Mérida, Yucatán, México.

Department of Archaeology, BioArCh, University of York, York, UK.

UMR 7209, Archéozoologie, Archéobotanique, Muséum

National d’Histoire Naturelle, Paris, France.

Research and Collections Center, Illinois State Museum, Springfield, IL, USA.

Touray & Meyer Veterinary Clinic, Serrekunda, Gambia.

Glenn A. Black

Laboratory of Anthropology, Indiana University Bloomington, Bloomington, IN, USA.

Department of Mammalogy, Museum of Comparative Zoology, Harvard University, Cambridge, MA, USA.

Department

of Chemical Engineering, University of Michigan, Ann Arbor, MI, USA.

Arctic & Antarctic Research Institute, St. Petersburg, Russia.

Department of Anthropology, Ohio State University, Columbus, OH,

USA.

Natural History Museum, University of Oslo, Oslo, Norway.

VNIIOkeangeologia Research Institute, St. Petersburg, Russia.

Center of Excellence in Paleontology, East Tennessee State University,

Gray, TN, USA.

Norwegian University of Science and Technology, University Museum, Trondheim, Norway.

Department of Archaeology , University of Aberdeen, Aberdeen, UK.

Department of

Anthropology , University of Illinois at Urbana-Champaign, Urbana-Champaign, IL, USA.

Carl R. Woese Institute for Genomic Biology, University of Illinois at Urbana-Champaign, Urbana-Champaign, IL,

USA.

School of Biological and Chemical Sciences, Queen Mary University of London, London, UK.

*These authors contributed equally to this work. †Deceased. ‡These authors cosupervised this work.

§Corresponding author. Email: [email protected] (L.A.F.F.); greger[email protected] (G.L.); [email protected] (E.P.M.)

on December 3, 2018 http://science.sciencemag.org/Downloaded from

a clade (PCD/Arctic) that is basal to both Western

Eurasian and East Asian dogs and suggests the

existence of a third monophyletic clade of dogs

(Fig. 1C). Although all three clades are well sup-

ported, the relationships between them are

ambiguous. For example, outgroup f 3 statis -

tics analysis (fig. S13) indicated that the PCD/

Arctic clade is basal to the two other Eurasian

dog clades. However, when we excluded specific

East Asian dogs that possess evidence of gene

flow from European dogs (table S7) (14), East

Asian dogs became the most basal clade in a

neighbor-joining tree and the PCD/Arctic clade

became the sister clade to Western Eurasian

dogs (fig. S11). Conversely, admixture graphs (3)

(fig. S25) and Treemix (18)(Fig.1D)suggested

that the PCD/Arctic clade is closest to East Asian

dogs and that Western Eurasian dogs are the

most basal. Conflicting phylogenies based on

nuclear data have been reported on numerous

occasions (1, 14, 16), and these inconsistent to-

pologies could result either from substantial post-

divergence gene flow among Eurasian dogs (Fig.

1C and fig. S25) (3, 14)orfromnearlysimulta-

neous divergence of all three lineages.

Our nuclear genome data indicate that mod-

ern Arctic dogs sampled from both Siberia and

North America cluster in a distinct phylogenetic

group that forms a sister taxon to PCDs (Fig. 1C).

This close phylogenetic relationship between mod-

ern American Arctic dogs (Alaskan malamutes,

Alaskan huskies, and Greenland dogs) and mod-

ern Eurasian Arctic dogs (Siberian huskies) (Fig.

1C and figs. S11 and S13) suggests that PCDs are

not the direct ancestor of modern American Arctic

dogs.ItispossiblethatmodernAmericanArctic

dogs are the descendants of dogs brought onto the

continent by the Paleo-Eskimos (~6000 years ago)

or by the Thule (~1000 years ago) (19). However,

both mitogenomic and low-coverage nuclear

data from a late Paleo-Eskimo dog from Kodiak

Island, Alaska (Uyak site sample AL3198) (Fig. 1A

Ní Leathlobhair et al., Science 361,81–85 (2018) 6 July 2018 2of5

Fig. 1. Sample locations and ancestry of PCDs. (A) A map depicting the

locations and ages of the archaeological remains analyzed in this study.

Each dot represents a single sample, and multiple samples per ar chaeological

site are grouped in bo xes. Sites mentioned in the tex t are labeled. BP, before

the present. (B) A tip-calibrated Bayesian mitochondrial phylogeneti c tree of

dogs within haplogroup A. This analysis was conducted with 66 nov el ancient

mitogenomes (all genomes with at least 10× coverage) together with 145

publicly available mitogen omes fro m both modern and ancient canids (3)

(fig. S6). Red branches r epr esent modern dogs, dark blue repr esents PCDs,

and light blue denotes ancient DNA from Arctic dogs. Blue bars on nodes

represent 95% HPD ages. The gray shaded area represents the time frame

during which people likely enter ed the Americas based on the age of

diverg ence between Native Americans and ancient Beringians (~20,000 years

ago) (12) and the flooding of the Bering land bridge (~11,000 years ago) (11).

graph constructed with Tr eemix (on the basis of transversions ) (3, 18)depicting

the relationship betw een PCDs [including the P ort au Choix (AL3194) and

Weyanoke Old Town (AL3223) samples] and other dog, wolf, and CTVT

populations. The scale bar shows 10 times the average standard error (s.e .) of

theentriesinthesamplecovariancematrix(18).

RESEARCH | REPORT

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and table S1), indicate that this dog was more

closely related to PCDs than to modern American

Arctic dogs (figs. S4 and S10). This finding sug-

gests that modern American Arctic dogs are not

the descendants of Paleo-Eskimo dogs and that

Paleo-Eskimos likely acquired local dogs in North

America or brought Siberian dogs that were

genetically indistinguishable from PCDs. Our

sampling did not include dogs from sites as-

sociated with the Thule culture, so it is plausible

that the modern American Arctic dogs included

in our analysis, such as Alaskan malamutes and

Greenland dogs, are the descendants of dogs

introduced by the Thule. Alternatively, the mod-

ernAmericanArcticdogsthatwesampledmay

be the descendants of recently introduced

Eurasian Arctic dogs, many of which were in-

troduced during the 19th-century Alaskan gold

rush and as sled dog racing stock (6).

Previous genomic analyses of the canine trans-

missible venereal tumor (CTVT) genome indicated

a close affinity with modern Arctic dogs (20).

CTVT is a contagious cancer clone that manifests

as genital tumors and spreads between dogs by

the transfer of living cancer cells during mating.

This clone first originated from the cells of an

individual dog, the “CTVT founder dog,” which

lived several thousand years ago, and the clone

still carries the genome of this individual (20).

To investigate the relationship between the

CTVT founder dog and PCDs, we analyzed two

CTVT genomes alongside a panel of modern and

ancient canid genomes.

Because CTVT is a cancer, and to limit the

impact of somatic mutations, we confined our

genotyping analysis to SNPs mapping to ge-

nomic regions that have retained both parental

chromosomal copies in CTVT (20) and excluded

singleton SNPs called exclusively in CTVT ge-

nomes and not found in any other canid genome.

CTVT clustered with PCDs on neighbor-joining

trees (Fig. 1C and figs. S10 and S11), a Bayesian

tree (fig. S12), Treemix (Fig. 1D), and admixture

graphs (fig. S25). This result is further supported

by both outgroup f3 statistics (fig. S13) and D

statistics (figs. S14 and S15). These findings indi-

cate that the CTVT founder dog is more closely

related to PCDs than to modern Arctic dogs.

Multiple horizontal transfers of mitochondrial

genomes from dog hosts to CTVT has led to the

replacement of the founder dog’s mitogenome

(21, 22); thus, we could not determine the mito-

chondrial haplogroup of the CTVT founder dog,

and we limited our analyses to the nuclear genome.

To assess whether the CTVT founder dog lived

before or after dogs entered North America, we

re-estimated its temporal origin by sequencing

the nuclear genomes of two CTVTs, 608T and

609T. 608T is a CTVT from the skin of a 10-month-

old puppy and was likely engrafted from the

mother’s vaginal tumor (609T) during birth. We

identified mutations generated by a clocklike

mutational process that were present in 608T but

not detectable in 609T and used these to derive

a lower bound for a somatic mutation rate for

CTVT (3). Applying this rate to the total burden

of clocklike somatic mutations in the CTVT lin-

eage (3), we estimated that the CTVT founde r

dog lived up to 8225 years ago (3). This time

frame postdates the initial arrival of dogs into

the Americas, raising the possibility that CTVT may

have originated in a dog living in North America.

To further assess this scenario, we quantified

the degree of introgression between canids en-

demic to North America (coyotes and North

Ní Leathlobhair et al., Science 361,81–85 (2018) 6 July 2018 3of5

Fig. 2. Legacy of PCDs in

modern American dogs.

(A) A map showing the

locations of dog populations

obtained from (9) and

their degrees of relatedness

(D statistics) to the

~4000-year-old Port au

Choix dog (AL3194) [see (3)

and fig. S14]. Higher values

(in red) represent closer

relatedness. The location of the

founder CTVT individual,

labeled in the plot, is unknown.

(B) A map depicting the

multiple introductions of dogs

into the Americas.

RESEARCH | REPORT

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American wolves), PCDs, modern Arctic dogs,

and the CTVT founder dog. Our analyses in-

dicated that, unlike Arctic dogs, PCDs share a

number of derived alleles with coyotes and

North American wolves, indicative of admixture

(figs. S16 and S17). The CTVT founder dog also

showed some weak evidence of coyote ancestry

but did not appear to possess admixture with

North American wolves (figs. S16 and S17). Be-

cause coyotes are restricted to North America,

this finding suggests that CTVT may have orig-

inated there. As we did not ascertain the degree

of coyote ancestry in ancient PCD-related dogs in

Northern Siberia (such as the Zhokhov Island

dogs) (Fig. 1), however, this analysis does not

establish the location in which CTVT originated.

Furthermore, studies that used somatic muta-

tions to reconstruct the phylogeography of the

CTVT clone indicated deep divergence in Asia

and rece nt introduction to the Americas (21).

Altogether, these results suggest a scenario in

which CTVT originated in Asia from a dog that

was closely related to PCDs, although we cannot

exclude the possibility that the clone arose in

America and then dispersed early into Asia be-

fore being reintro duced to America.

ThelegacyofPCDsinmodernAmericancanid

populations is uncertain. It has been suggested

that some North American wolves obtained a

mutation leading to black coat color possib ly via

admixture with early American dogs (23). This

allele was not present, however, in either of the

two higher-coverage ancient PCDs in this study

(3)orinCTVT(20). Additional ancient genomes

are necessary to determine if this allele was

present in the PCD population.

In addition, previous studies have argued that

some modern American dog populations possess

a genetic signature fromindigenousAmerican

dogs (8, 9, 24). To test this hypothesis, we

analyzed nuclear data obtained from more than

5000 modern dogs (including American village

dogs) genotyped on a 180,000 SNP array (9).

We found 7 to 20% PCD ancestry in modern

American Arctic dogs (Alaskan huskies, Alaskan

malamutes, and Greenland dogs) by using f4

ratios (tables S10 and S11) (3). This result, how-

ever, may reflect ancient population substructure

in Arctic dogs rather than genuine admixture (3).

Our f4 ratio analysis did not detect a significant

admixture signal from PCDs in any modern

American dogs of European ancestry (table S10).

Our admixture analysis detected varying de-

grees (0 to 33%) of PCD/Arctic ancestry in three

individual Carolina dogs (fig. S20). This analysis,

however, could not distinguish between PCD and

Arctic ancestry, and we cannot rule out that this

signal was a result of admixture from modern

Arctic dogs and not from PCDs (3). The majority

of modern American dog populations, including

138 village dogs from South America and mul-

tiple “native” breeds (e.g., hairless dogs and

Catahoulas), possess no detectable traces of PCD

ancestry (Fig. 2A, fig. S20, and table S10), though

this analysis may suffer from ascertainment bias.

To further assess the contribution of PCDs

to modern American dog populations, we also

analyzed 590 additional modern dog mitoge-

nomes, including those from 169 village and

breed dogs that were sampled in North and

South America (21). We identified two modern

American dogs (a chihuahua and a mixed-breed

dog from Nicaragua) that carried PCD mito-

chondrial haplotypes (fig. S5), consistent with

a limited degree of PCD ancestry (<2%) in

modern American dogs. We also identified

three East Asian dogs that carried a PCD hap-

lotype, possibly as a result of ancient population

substructure or recent dog dispersal (fig. S5) (3).

Although greater degrees of PCD ancestry may

remain in American dogs that have not yet been

sampled, our results suggest that European dogs

almost completely replaced native American dog

lineages. This near disappea rance of PCDs likely

resulted from the arrival of Europeans, which led

to shifts in cultural preferences and the per-

secution of indigenous dogs (25). Introduced

European dogs may also have brought infectious

diseases to which PCDs were susceptible.

The first appearance of dogs in the North Amer-

ican archaeological record occurred ~4500 years

after the earliest evidence of human activity on

the continent (4, 11). In addition, our molecular

clock analysis indicates that the PCD lineage ap-

peared ~6500 years after North American human

lineages (Fig. 1B) (10). These discrepancies suggest

that dogs may not have arrived into the Americas

alongside

the very first human migration but

were instead potentially part of a later arrival (12)

before the flooding of the Bering land bridge

~11,000 years ago (11). This timing is compati-

ble with both the archaeological record and our

PCD divergence time estimate and suggests a

scenario in which dogs were brought to the

Americas several thousand years after the first

people arrived there.

This initial dog population entered North

America and then dispersed throughout the

Americas, where it remained isolated for at least

9000 years. Within the past 1000 years, however ,

at leas t three independent reintroductions of

dogs have occurred. The first may have consisted

of Arctic dogs that arrived with the Thule culture

~1000 years ago (6). Then, beginning in the 15th

century, Europeans brought a second wave of

dogs that appear to have almost completely re-

placed native dogs. Lastly, Siberian huskies were

introduced to the American Arctic during the

Alaskan gold rush (25). As a result of these more

recent introductions, the modern American dog

population is largely derived from Eurasian breeds,

and the closest known extant vestige of the first

American dogs now exists as a worldwide trans-

missible cancer.

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AC KN OW LE D GM E NT S

We thank L. Orlando, R. K. Wayne, and D. Meltzer for their valuable

comments; B. M. Kemp, M. Masson, and J. Chupasko for support;

and J. Southon (W. M. Keck Carbon Cycle Accelerator Mass

Spectrometry Laboratory, University of California, Irvine) for the

radiocarbon date on the Port au Choix dog. We acknowledge the

University of Oxford Advanced Research Computing (ARC) facility

for providing computing time. We thank the Illinois State Museum,

the Illinois State Archaeological Survey, the Glenn A. Black

Laboratory of Archaeology at Indiana University Bloomington, the

Instituto Nacional de Antropologia e Historia, and the Ohio

Historical Society for access to material. We thank The Rooms

(Museum Division), the Board Executive, and the Government of

Newfoundland and Labrador for permission to access and sample

the Port au Choix material. We are grateful to M. Ptaszynska for

useful information and to S. Zhang for assistance with samples. We

thank the staff of the Danish National High-throughput Sequencing

Centre for assistance in data generation. Funding: L.A.F.F. was

supported by the Wellcome Trust (210119/Z/18/Z) and by Wolfson

College (University of Oxford). L.A.F.F., J.H., A.L., A.H.-B., O.L.,

K.M.D., and G.L. were supported by a European Research Council

grant (ERC-2013-StG-337574-UNDEAD) or Natural Environmental

Research Council grants (NE/K005243/1 and NE/K003259/1)

or both. M.N.L. and E.P.M. were supported by Wellcome

(102942/Z/13/A) and a Philip Leverhulme Prize awarded by the

Leverhulme Trust. A.R.P. was supported by the Max Planck

Society. E.K.I.-P. was supported by a Clarendon Fund scholarship

from the University of Oxford. M.T.P.G. was supported by a

European Research Council grant (ERC-2015-CoG-681396–

Extinction Genomics). A.M. was supported by the Muséum National

d’Histoire Naturelle. K.E.W. and R.S.M. were supported by an NSF

grant (BCS-1540336) and a Wenner-Gren grant. V.G. was

supported by a Social Sciences and Humanities Research Council

Insight grant. V.V.P., E.Y.P., and P.A.N. were supported by Russian

Science Foundation project N16-18-10265-RNF. Y.-M.K. was

supported by a Herchel Smith research fellowship. S.J.C. was

supported by Millennia Research. J.J. was supported by the Santa

Barbara Museum of Natural History. A.R.B. was supported by the

American Kennel Club and the NIH. We thank the Illinois State

Museum Society for funding. Author contributions: L.A.F.F., G.L.,

and E.P.M. conceived of the project and designed the research;

A.R.P., K.M.D., and G.L. coordinated the archaeological analyses

and sample collection efforts with input from R.S.M., C.A., A.H.-B.,

and K.E.W.; A.R.P., C.A., J.B., E.G., A.J.H., M.-H.S.S., S.J.C., M.E.,

Y.N.C., V.G., J.J., A.K.K., P.A.N., C.P.L., A.M., T.M., K.N.M., M.O.,

E.Y.P., P.S., V.V.I., C.W., and V.V.P. provided and/or collected

samples; K.E.W., A.L., J.H., O.L., S.B., A.D., E.A.D., J.E., J.-M.R.,

and M.-H.S.S. conducted the ancient laboratory work with input

from R.S.M., G.L., L.A.F.F., E.W., I.B., and M.T.P.G.; M.M., E.P.M.,

and A.S. provided and/or collected CTVT samples; M.N.L. and

Y.-M.K. conducted the CTVT analyses with input from E.P.M., K.G.,

and L.A.F.F.; M.N.L., L.A.F.F., and E.K.I.-P. conducted the analyses

of ancient data with input from S.G., A.K., A.R.B., and E.P.M.;

and L.A.F.F., G.L., E.P.M., M.N.L., and A.R.P. wrote the paper with

input from all other authors. Competing interests: A.D., J.E.,

and J.-M.R. are employees of Arbor Biosciences, which provided

target enrichment kits used in this study. J.-M.R. is also a founder

of Arbor Biosciences. A.R.B. is the founder and chief strategy

Ní Leathlobhair et al., Science 361,81–85 (2018) 6 July 2018 4of5

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officer of Embark Veterinary. K.M.D. currently holds honorary

professor positions in the departments of archaeology at both the

University of Aberdeen and Simon Fraser University. Data and

materials availability: The reads for the ancient data have been

deposited at the European Nucleotide Archive (ENA) with project

number PRJEB22026. Reads for new CTVT genomes were

deposited at the European Nucleotide Archive (ENA) with project

number PRJEB22148. Mitochondrial sequence alignments,

genotype files (in plink format), and phylogenetic trees were

deposited in Dryad (26).

SUPPLEMENTARY MATERIALS

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Materials and Methods

Figs. S1 to S27

Tables S1 to S16

References (27–180)

13 September 2017; resubmitted 26 December 2017

Accepted 10 May 2018

10.1126/science.aao4776

Ní Leathlobhair et al., Science 361,81–85 (2018) 6 July 2018 5of5

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The evolutionary history of dogs in the Americas

Elizabeth P. Murchison, Greger Larson and Laurent A. F. Frantz

Christopher Widga, Eske Willerslev, Vladimir V. Pitulko, Ian Barnes, M. Thomas P. Gilbert, Keith M. Dobney, Ripan S. Malhi,

Jean-Marie Rouillard, Elena Y. Pavlova, Paul Sciulli, Mikkel-Holger S. Sinding, Andrea Strakova, Varvara V. Ivanova,

Pavel A. Nikolskiy, Carlos Peraza Lope, Aurélie Manin, Terrance Martin, Michael Meyer, Kelsey Noack Myers, Mark Omura,

Guiry, Anders J. Hansen, Ardern Hulme-Beaman, John Johnson, Andrew Kitchen, Aleksei K. Kasparov, Young-Mi Kwon,

Devault, Evangelos A. Dimopoulos, Morley Eldridge, Jacob Enk, Shyam Gopalakrishnan, Kevin Gori, Vaughan Grimes, Eric

Lebrasseur, Carly Ameen, Jeffrey Blick, Adam R. Boyko, Selina Brace, Yahaira Nunes Cortes, Susan J. Crockford, Alison

Máire Ní Leathlobhair, Angela R. Perri, Evan K. Irving-Pease, Kelsey E. Witt, Anna Linderholm, James Haile, Ophelie

DOI: 10.1126/science.aao4776

(6397), 81-85.361Science

, this issue p. 81; see also p. 27Science

transmissible venereal tumor.

have been mostly replaced by dogs introduced by Europeans, with the primary extant lineage remaining as a canine

date back to a common ancestor that coincides with the first human migrations across Beringia. This lineage appears to

not domesticated from North American wolves but likely originated from a Siberian ancestor. Furthermore, these lineages

nuclear genomes of ancient dogs (see the Perspective by Goodman and Karlsson). The earliest New World dogs were

sequenced the mitochondrial andet al.and populations reflect their introduction to the New World, Ní Leathlobhair

Dogs have been present in North America for at least 9000 years. To better understand how present-day breeds

Lineage losses for man's best friend

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MATERIALS

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REFERENCES

http://science.sciencemag.org/content/361/6397/81#BIBL

This article cites 119 articles, 27 of which you can access for free

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on December 3, 2018 http://science.sciencemag.org/Downloaded from