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Genetic structure in village dogs reveals a Central Asian domestication origin

Laura M. Shannon, Ryan H. Boyko, Marta Castelhano, Elizabeth Corey, Jessica J. Hayward, Corin McLean, Michelle E. White, Mounir Abi Said, Baddley A. Anita, Nono Ikombe Bondjengo, Jorge Calero, Ana Galov, Marius Hedimbi, Bulu Imam, Rajashree Khalap, Douglas Lally, Andrew Masta, Kyle C. Oliveira, Lucía Pérez, Julia Randall, Nguyen Minh Tam, Francisco J. Trujillo-Cornejo, Carlos Valeriano, Nathan B. Sutter, Rory J. Todhunter, Carlos D. Bustamante, and Adam R. Boyko
PNAS published ahead of print October 19, 2015 https://doi.org/10.1073/pnas.1516215112
Laura M. Shannon
aDepartment of Biomedical Sciences, Cornell University, Ithaca, NY 14853;
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Ryan H. Boyko
bDepartment of Epidemiology of Microbial Diseases, Yale School of Public Health, Yale University, New Haven, CT 06510;
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Marta Castelhano
cDepartment of Clinical Sciences, Cornell University, Ithaca, NY 14853;
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Elizabeth Corey
cDepartment of Clinical Sciences, Cornell University, Ithaca, NY 14853;
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Jessica J. Hayward
aDepartment of Biomedical Sciences, Cornell University, Ithaca, NY 14853;
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Corin McLean
dBiogen Idec, Cambridge, MA 02142;
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Michelle E. White
aDepartment of Biomedical Sciences, Cornell University, Ithaca, NY 14853;
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Mounir Abi Said
eBiology Department, American University of Beirut, Beirut, Lebanon;
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Baddley A. Anita
fHoniara Veterinary Clinic and Surgery, Honiara, Solomon Islands;
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Nono Ikombe Bondjengo
gDépartement de l’environnement, Faculté des Sciences, Université de Mbandaka, Mbandaka, Democratic Republic of Congo;
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Jorge Calero
hAcadémico de Arqueologia, Universidad Nacional de San Antonio Abad del Cusco, Cusco, Peru;
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Ana Galov
iDepartment of Animal Physiology, University of Zagreb, Zagreb 10000, Croatia;
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Marius Hedimbi
jMicrobiology, University of Namibia, Windhoek, Namibia;
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Bulu Imam
kSanskriti Centre, Hazaribagh, Jharkhand, India 825 301;
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Rajashree Khalap
lThe INDog Project, Maharashtra, India;
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Douglas Lally
mThe Mongolian Bankhar Project, Ulaanbaatar, Mongolia;
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Andrew Masta
nSchool of Medicine and Health Sciences, University of Papua New Guinea, Boroko, Port Moresby, National Capital District, 111, Papua New Guinea;
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Kyle C. Oliveira
aDepartment of Biomedical Sciences, Cornell University, Ithaca, NY 14853;
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Lucía Pérez
oInstituto de Biología, Universidad Nacional Autónoma de México, Mexico City, Federal District, Mexico;
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Julia Randall
pUniversity of Massachusetts Medical School, Worcester, MA 01655;
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Nguyen Minh Tam
qVietnam National Museum of Nature, Vietnam Academy of Science and Technology, Hanoi, Vietnam;
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Francisco J. Trujillo-Cornejo
oInstituto de Biología, Universidad Nacional Autónoma de México, Mexico City, Federal District, Mexico;
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Carlos Valeriano
hAcadémico de Arqueologia, Universidad Nacional de San Antonio Abad del Cusco, Cusco, Peru;
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Nathan B. Sutter
rDepartment of Biology, La Sierra University, Riverside, CA 92505;
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Rory J. Todhunter
cDepartment of Clinical Sciences, Cornell University, Ithaca, NY 14853;
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Carlos D. Bustamante
sDepartment of Genetics, Stanford University School of Medicine, Stanford, CA 94305
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Adam R. Boyko
aDepartment of Biomedical Sciences, Cornell University, Ithaca, NY 14853;
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  • For correspondence: boyko@cornell.edu
  1. Edited by David M. Hillis, The University of Texas at Austin, Austin, TX, and approved September 11, 2015 (received for review August 19, 2015)

This article has a reply. Please see:

  • Questioning the evidence for a Central Asian domestication origin of dogs
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Significance

Dogs were the first domesticated species, but the precise timing and location of domestication are hotly debated. Using genomic data from 5,392 dogs, including a global set of 549 village dogs, we find strong evidence that dogs were domesticated in Central Asia, perhaps near present-day Nepal and Mongolia. Dogs in nearby regions (e.g., East Asia, India, and Southwest Asia) contain high levels of genetic diversity due to their proximity to Central Asia and large population sizes. Indigenous dog populations in the Neotropics and South Pacific have been largely replaced by European dogs, whereas those in Africa show varying degrees of European vs. indigenous African ancestry.

Abstract

Dogs were the first domesticated species, originating at least 15,000 y ago from Eurasian gray wolves. Dogs today consist primarily of two specialized groups—a diverse set of nearly 400 pure breeds and a far more populous group of free-ranging animals adapted to a human commensal lifestyle (village dogs). Village dogs are more genetically diverse and geographically widespread than purebred dogs making them vital for unraveling dog population history. Using a semicustom 185,805-marker genotyping array, we conducted a large-scale survey of autosomal, mitochondrial, and Y chromosome diversity in 4,676 purebred dogs from 161 breeds and 549 village dogs from 38 countries. Geographic structure shows both isolation and gene flow have shaped genetic diversity in village dog populations. Some populations (notably those in the Neotropics and the South Pacific) are almost completely derived from European stock, whereas others are clearly admixed between indigenous and European dogs. Importantly, many populations—including those of Vietnam, India, and Egypt—show minimal evidence of European admixture. These populations exhibit a clear gradient of short-range linkage disequilibrium consistent with a Central Asian domestication origin.

  • admixture
  • domestication
  • linkage disequilibrium
  • introgression
  • haplotype diversity

Footnotes

  • ↵1To whom correspondence should be addressed. Email: boyko{at}cornell.edu.
  • Author contributions: R.H.B., J.C., A.G., D.L., N.B.S., R.J.T., C.D.B., and A.R.B. designed research; L.M.S., R.H.B., M.C., E.C., J.J.H., C.M., M.E.W., M.A.S., B.A.A., N.I.B., J.C., A.G., M.H., B.I., R.K., D.L., A.M., K.C.O., L.P., J.R., N.M.T., F.J.T.-C., C.V., N.B.S., R.J.T., and A.R.B. performed research; L.M.S. and A.R.B. analyzed data; and L.M.S. and A.R.B. wrote the paper.

  • Conflict of interest statement: A.R.B. and R.H.B. are cofounders and officers of Embark Veterinary, Inc., a canine genetics testing company.

  • This article is a PNAS Direct Submission.

  • Data deposition: Genotype and geographical data have been deposited in Dryad, datadryad.org (doi:10.5061/dryad.v9t5h).

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1516215112/-/DCSupplemental.

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Dog genetic diversity reveals Central Asian origin
Laura M. Shannon, Ryan H. Boyko, Marta Castelhano, Elizabeth Corey, Jessica J. Hayward, Corin McLean, Michelle E. White, Mounir Abi Said, Baddley A. Anita, Nono Ikombe Bondjengo, Jorge Calero, Ana Galov, Marius Hedimbi, Bulu Imam, Rajashree Khalap, Douglas Lally, Andrew Masta, Kyle C. Oliveira, Lucía Pérez, Julia Randall, Nguyen Minh Tam, Francisco J. Trujillo-Cornejo, Carlos Valeriano, Nathan B. Sutter, Rory J. Todhunter, Carlos D. Bustamante, Adam R. Boyko
Proceedings of the National Academy of Sciences Oct 2015, 201516215; DOI: 10.1073/pnas.1516215112

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Dog genetic diversity reveals Central Asian origin
Laura M. Shannon, Ryan H. Boyko, Marta Castelhano, Elizabeth Corey, Jessica J. Hayward, Corin McLean, Michelle E. White, Mounir Abi Said, Baddley A. Anita, Nono Ikombe Bondjengo, Jorge Calero, Ana Galov, Marius Hedimbi, Bulu Imam, Rajashree Khalap, Douglas Lally, Andrew Masta, Kyle C. Oliveira, Lucía Pérez, Julia Randall, Nguyen Minh Tam, Francisco J. Trujillo-Cornejo, Carlos Valeriano, Nathan B. Sutter, Rory J. Todhunter, Carlos D. Bustamante, Adam R. Boyko
Proceedings of the National Academy of Sciences Oct 2015, 201516215; DOI: 10.1073/pnas.1516215112
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