Abstract

Advances in genome technology have facilitated a new understanding of the historical and genetic processes crucial to rapid phenotypic evolution under domestication1,2. To understand the process of dog diversification better, we conducted an extensive genome-wide survey of more than 48,000 single nucleotide polymorphisms in dogs and their wild progenitor, the grey wolf. Here we show that dog breeds share a higher proportion of multi-locus haplotypes unique to grey wolves from the Middle East, indicating that they are a dominant source of genetic diversity for dogs rather than wolves from east Asia, as suggested by mitochondrial DNA sequence data3. Furthermore, we find a surprising correspondence between genetic and phenotypic/functional breed groupings but there are exceptions that suggest phenotypic diversification depended in part on the repeated crossing of individuals with novel phenotypes. Our results show that Middle Eastern wolves were a critical source of genome diversity, although interbreeding with local wolf populations clearly occurred elsewhere in the early history of specific lineages. More recently, the evolution of modern dog breeds seems to have been an iterative process that drew on a limited genetic toolkit to create remarkable phenotypic diversity.

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Acknowledgements

Grants from NSF and NIH (R.K.W.; C.D.B. and J.N.), the Polish Ministry of Science and Higher Education (M.P. and W.J.), European Nature Heritage Fund EURONATUR (W.J.), National Basic Research Program of China (Y.-p.Z.), and Chinese Academy of Sciences (Y.-p.Z.) supported this research. J.N. was supported by the Searle Scholars Program. B.M.vH. was supported by a NIH Training Grant in Genomic Analysis and Interpretation. K.E.L. was supported by a NSF Graduate Research Fellowship. E.A.O., D.S.M., T.C.S., A.E. and H.G.P. are supported by the intramural program of the National Human Genome Research Institute. M.P. was supported by the Foundation for Polish Science. Wolf samples from central and eastern Europe and Turkey were collected as a result of a continuing project on genetic differentiation in Eurasian wolves. We thank the project participants (B. Jedrzejewska, V. E. Sidorovich, M. Shkvyrya, I. Dikiy, E. Tsingarskaya and S. Nowak) for their permission to use 72 samples for this study. We acknowledge R. Hefner and the Zoological collection at Tel Aviv University for Israeli wolf samples. We thank the American Kennel Club (AKC) for the dog images reproduced in Fig. 1. We also gratefully acknowledge the dog owners who generously provided samples, the AKC Canine Health Foundation, and Affymetrix Corporation. We thank B. Van Valkenburgh, K.-P. Koepfli, D. Stahler and D. Smith for reviewing the manuscript.

Author Contributions Samples were contributed by E.G., M.P., W.J., C.G., E.R., D.B., A.W., J.S., M.M., E.A.O. and R.K.W. The experiment was designed and carried out with the help of B.M.vH., J.P.P., H.G.P., P.Q., D.S.M., T.C.S., A.E., A.W., J.S., M.C., P.G.J., Z.Q., W.H., Z.-L.D., Y.-p.Z., C.D.B., E.A.O. and R.K.W. The genotyping program was written by A.R.B., A.A., A.R., K.B., A.B. and C.D.B. and further programming was completed by K.E.L., J.D.D., D.A.E., E.H. and J.N. The analyses were conducted by B.M.vH., J.P.P., K.E.L., E.H., H.G.P., J.D.D., A.R.B., D.A.E., A.A., A.R., J.C.K. and J.N. The manuscript was written by B.M.vH., K.E.L., C.D.B., E.A.O., J.N. and R.K.W.

Author information

Affiliations

  1. Department of Ecology and Evolutionary Biology, 621 Charles E. Young Drive South, University of California, Los Angeles, California 90095, USA

    • Bridgett M. vonHoldt
    • , John P. Pollinger
    • , James C. Knowles
    • , John Novembre
    •  & Robert K. Wayne
  2. Department of Biological Statistics and Computational Biology, Cornell University, Ithaca, New York 14853-2601, USA

    • Kirk E. Lohmueller
    • , Jeremiah D. Degenhardt
    • , Adam R. Boyko
    • , Adam Auton
    • , Andy Reynolds
    • , Kasia Bryc
    • , Abra Brisbin
    •  & Carlos D. Bustamante
  3. Department of Biostatistics, University of California, Los Angeles, California 14853, USA

    • Eunjung Han
  4. Cancer Genetics Branch, National Human Genome Research Institute, National Institutes of Health, Bethesda, Maryland 20892, USA

    • Heidi G. Parker
    • , Pascale Quignon
    • , Dana S. Mosher
    • , Tyrone C. Spady
    • , Abdel Elkahloun
    •  & Elaine A. Ostrander
  5. Department of Biomolecular Engineering, University of California, Santa Cruz, California 95064, USA

    • Dent A. Earl
  6. Department of Zoology, Tel Aviv University, Tel Aviv 69978, Israel

    • Eli Geffen
  7. Museum and Institute of Zoology, Polish Academy of Sciences, Wilcza 64, 00-679 Warszawa, Poland

    • Malgorzata Pilot
  8. Mammal Research Institute, Polish Academy of Sciences, 17-230 Bialowieza, Poland

    • Wlodzimierz Jedrzejewski
  9. Instituto Superiore per la Protezione e la Ricerca Ambientale (ISPRA), 40064 Ozzano Emilia (B), Italy

    • Claudia Greco
    •  & Ettore Randi
  10. Department of Population Health and Reproduction, School of Veterinary Medicine, University of California, Davis, California 95616, USA

    • Danika Bannasch
  11. School of Biotechnology and Biomolecular Sciences and Clive and Vera Ramaciotti Center for Gene Function Analysis, University of New South Wales, Sydney NSW 2052, Australia

    • Alan Wilton
    •  & Jeremy Shearman
  12. Faculty of Environmental Design, University of Calgary, 2500 University Drive NW, Calgary, Alberta T2N 1N4, Canada

    • Marco Musiani
  13. Affymetrix Corporation, 3420 Central Expressway, Santa Clara, California 95051, USA

    • Michelle Cargill
  14. The WALTHAM Centre for Pet Nutrition, Waltham on the Worlds, Leicestershire LE14 4RT, UK

    • Paul G. Jones
  15. Affymetrix Asia Pacific, Scientific Affairs and Collaborations, 1233 Lujiazui Ring Road, AZIA Center, Suite 1508, Shanghai 200120, China

    • Zuwei Qian
    •  & Wei Huang
  16. Laboratory for Conservation and Utilization of Bio-resources, Yunnan University, Kunming 650091, China

    • Zhao-Li Ding
  17. State Key Laboratory of Genetic Resources and Evolution, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming 650223, China

    • Ya-ping Zhang
  18. Interdepartmental Program in Bioinformatics, 621 Charles E. Young Drive South, University of California, Los Angeles, California 90095, USA

    • John Novembre

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Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Robert K. Wayne.

Supplementary information

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    Supplementary Information

    This file contains Supplementary Notes A - C with References, Supplementary Tables 1-7 and Supplementary Figures 1-18 with Legends.

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