To identify genetic changes underlying dog domestication and reconstruct their early evolutionary history, we generated high-quality genome sequences from three gray wolves, one from each of the three putative centers of dog domestication, two basal dog lineages (Basenji and Dingo) and a golden jackal as an outgroup. Analysis of these sequences supports a demographic model in which dogs and wolves diverged through a dynamic process involving population bottlenecks in both lineages and post-divergence gene flow. In dogs, the domestication bottleneck involved at least a 16-fold reduction in population size, a much more severe bottleneck than estimated previously. A sharp bottleneck in wolves occurred soon after their divergence from dogs, implying that the pool of diversity from which dogs arose was substantially larger than represented by modern wolf populations. We narrow the plausible range for the date of initial dog domestication to an interval spanning 11–16 thousand years ago, predating the rise of agriculture. In light of this finding, we expand upon previous work regarding the increase in copy number of the amylase gene (AMY2B) in dogs, which is believed to have aided digestion of starch in agricultural refuse. We find standing variation for amylase copy number variation in wolves and little or no copy number increase in the Dingo and Husky lineages. In conjunction with the estimated timing of dog origins, these results provide additional support to archaeological finds, suggesting the earliest dogs arose alongside hunter-gathers rather than agriculturists. Regarding the geographic origin of dogs, we find that, surprisingly, none of the extant wolf lineages from putative domestication centers is more closely related to dogs, and, instead, the sampled wolves form a sister monophyletic clade. This result, in combination with dog-wolf admixture during the process of domestication, suggests that a re-evaluation of past hypotheses regarding dog origins is necessary.

This work was supported by an NSF Postdoctoral Fellowship DBI-0905784 (AHF), NSF Graduate Research Fellowship (RMS), Searle Foundation Scholar Award (JN), NSF grant EF-1021397 (JN RKW AHF RMS EH), NIH T32 HG002536 (EH), NIH (NIGMS) grant GM102192 (IG AS), UC MEXUS-CONACYT doctoral fellowship 213627 (DODV), PhD grant from Fundaçao para a Ciéncia e a Tecnologia (Portugal) SFRH/BD/60549/2009 (PMS), PhD Grant from University of Bologna (Italy), XXIV cicle, Biodiversity and Evolution (MG), National Science and Technology Support Project of China 2012BAC01B06 (ZF), Rosztoczy Foundation (PM), US HHS Ruth L. Kirschstein Institutional National Research Service Award #T32 CA009056 (KS), National Institute of Bioinformatics (BLG), Intramural Program of the National Human Genome Research Institute (HB HGP EAO), JAEDOC-CSIC (EFS) (OR), Marie Curie CIG PCIG10-GA-2011-303772 (CA) Programa de Captación del Conocimiento para Andalucía-a for sequencing of Chinese wolf at BGI, ERC Starting Grant 260372 and MICINN (Spain) BFU2011-28549 (TMB), and NSF grant DEB-0948510 (ARB CDB). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript