Origins and genetic legacy of prehistoric dogs

Abstract

Dogs were the first domestic animal, but little is known about their population history and to what extent it was linked to humans. We sequenced 27 ancient dog genomes and found that all dogs share a common ancestry distinct from present-day wolves, with limited gene flow from wolves since domestication but substantial dog-to-wolf gene flow. By 11,000 years ago, at least five major ancestry lineages had diversified, demonstrating a deep genetic history of dogs during the Paleolithic. Coanalysis with human genomes reveals aspects of dog population history that mirror humans, including Levant-related ancestry in Africa and early agricultural Europe. Other aspects differ, including the impacts of steppe pastoralist expansions in West and East Eurasia and a near-complete turnover of Neolithic European dog ancestry.

Figure 1. Genomic structure of dogs dates to the Pleistocene.

A) Sampling locations of ancient dogs. B) Principal components analysis on all possible f₄-statistics among ancient dogs (gray) and a selection of worldwide modern dogs. C) Outgroup f ₃-statistics reveal a cline of Levant versus Baikal (horizontal and vertical axes, respectively) related ancestry across ancient west Eurasian dogs, but not among modern European dogs. D) Coalescent simulations demonstrating that a diagonal f ₃-cline as in panel C is consistent with an admixture event, but less so with continuous gene flow and not with phylogenetic structure alone. E) An admixture graph that fits all f₄-statistics between major dog lineages. The European dog was grafted onto the graph identified through exhaustive testing.

Fig. 2. All detectable gene flow is consistent with being unidirectional from dogs into wolf populations.

A) Illustration of asymmetry tests (f ₄-statistics) comparing 35 Eurasian gray wolves to all pairs of 66 ancient and modern dogs. B) Selected results using Coyote as outgroup. C) A wolf from Xinjiang, western China, is not closer to some dog populations than to others, as the test statistics are consistent with being normally distributed around 0 (the quantile-quantile plot includes all 66 dogs). If there was a substantial gene flow from some wolf population into some dog population, we would expect all wolf individuals to display asymmetric relationships.

Figure 3. Quantitative comparisons between dog and human population genomic structure.

A) Principal components analysis on all possible f ₄-statistics on ancient dogs (blue), overlaid through Procrustes transformation by the corresponding analysis performed on ancient humans matched in time, space, and cultural context to the dogs (green). Dashed lines connect each matched pair. B) Euclidian residuals between the Procrustes-rotated human and dog coordinates. C) The three admixture graphs that fit for one species and provide the smallest error for the other. Scatter plots show absolute Z-scores for the difference between observed and predicted f₄-statistics. D) Examples of f₄-statistics that reveal similarities and differences between humans and dogs (far right text).

Figure 4. Expansion of copy number in the AMY2B pancreatic amylase gene largely occurred after the transition to agriculture.

Ancient dogs are plotted against their age, with blue color indicating dogs from likely hunter-gatherer human contexts. Bars denote 95% binomial confidence intervals around the ratio of the number of reads mapping to the copy number variable region to those mapping to control regions throughout the genome.

Figure 5. Ancestry of global dogs today.

A) For each present-day population, the ancestry proportions estimated by the best-fitting qpAdm model, restricted to models containing up to four of seven selected sources, are displayed. Populations for which a single component accounts for ≥98% of the ancestry are collapsed to smaller circles. Dog pictures were obtained from Wikimedia under the CC BY-SA 3.0 license (https://commons.wikimedia.org/wiki/Special:ListFiles/Desaix83). B) Illustrations of inferred population histories in three regions of the world.