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Genome-wide SNP and haplotype analyses reveal a rich history underlying dog domestication

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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Figure 1: Neighbour-joining trees of domestic dogs and grey wolves.
Figure 2: Genome-wide analysis of SNP variation in domestic dogs and grey wolves.

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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.

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Correspondence to Robert K. Wayne.

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This file contains Supplementary Notes A - C with References, Supplementary Tables 1-7 and Supplementary Figures 1-18 with Legends. (PDF 12650 kb)

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vonHoldt, B., Pollinger, J., Lohmueller, K. et al. Genome-wide SNP and haplotype analyses reveal a rich history underlying dog domestication. Nature 464, 898–902 (2010). https://doi.org/10.1038/nature08837

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