Genome Sequencing Highlights the Dynamic Early History of Dogs

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.

[1]  James A. Cuff,et al.  Genome sequence, comparative analysis and haplotype structure of the domestic dog , 2005, Nature.

[2]  Robert L. Beschta,et al.  Trophic cascades in Yellowstone: The first 15 years after wolf reintroduction , 2012 .

[3]  Catherine André,et al.  Coat Variation in the Domestic Dog Is Governed by Variants in Three Genes , 2009, Science.

[4]  M. DePristo,et al.  The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. , 2010, Genome research.

[5]  Leif Andersson,et al.  Rethinking dog domestication by integrating genetics, archeology, and biogeography , 2012, Proceedings of the National Academy of Sciences.

[6]  J. Vigne,et al.  New evidence for Upper Palaeolithic small domestic dogs in South-Western Europe , 2011 .

[7]  A. Boyko,et al.  Artificial selection on brain-expressed genes during the domestication of dog. , 2013, Molecular biology and evolution.

[8]  D. Haussler,et al.  Evolutionarily conserved elements in vertebrate, insect, worm, and yeast genomes. , 2005, Genome research.

[9]  C. Russo,et al.  The evolution of South American endemic canids: a history of rapid diversification and morphological parallelism , 2010, Journal of evolutionary biology.

[10]  Jeremiah D. Degenhardt,et al.  Complex population structure in African village dogs and its implications for inferring dog domestication history , 2009, Proceedings of the National Academy of Sciences.

[11]  Sudhir Kumar,et al.  Mutation rates in mammalian genomes , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[12]  M. Hofreiter,et al.  Fossil dogs and wolves from Palaeolithic sites in Belgium, the Ukraine and Russia: osteometry, ancient DNA and stable isotopes , 2009 .

[13]  N. Rooney,et al.  Ádám Miklósi Dog Behaviour, Evolution, and Cognition , 2008, Animal Behaviour.

[14]  J. van der Plicht,et al.  A 33,000-Year-Old Incipient Dog from the Altai Mountains of Siberia: Evidence of the Earliest Domestication Disrupted by the Last Glacial Maximum , 2011, PloS one.

[15]  M. Jakobsson,et al.  Estimation of population divergence times from non-overlapping genomic sequences: examples from dogs and wolves. , 2011, Molecular biology and evolution.

[16]  J. Kitzman,et al.  Personalized Copy-Number and Segmental Duplication Maps using Next-Generation Sequencing , 2009, Nature Genetics.

[17]  A. Siepel,et al.  Bayesian inference of ancient human demography from individual genome sequences , 2011, Nature Genetics.

[18]  K. Lindblad-Toh,et al.  The genomic signature of dog domestication reveals adaptation to a starch-rich diet , 2013, Nature.

[19]  Christopher C Wilmers,et al.  Wolves-coyotes-foxes: a cascade among carnivores. , 2012, Ecology.

[20]  Chung-I Wu,et al.  The genomics of selection in dogs and the parallel evolution between dogs and humans , 2013, Nature Communications.

[21]  Philip L. F. Johnson,et al.  A Draft Sequence of the Neandertal Genome , 2010, Science.

[22]  K. Lindblad-Toh,et al.  Efficient mapping of mendelian traits in dogs through genome-wide association , 2007, Nature Genetics.

[23]  R. Wayne,et al.  Megafaunal Extinctions and the Disappearance of a Specialized Wolf Ecomorph , 2007, Current Biology.

[24]  Martina Lázničková-Galetová,et al.  Palaeolithic dog skulls at the Gravettian Předmostí site, the Czech Republic , 2012 .

[25]  Joseph K. Pickrell,et al.  Inference of Population Splits and Mixtures from Genome-Wide Allele Frequency Data , 2012, PLoS genetics.

[26]  E. Matisoo-Smith,et al.  A detailed picture of the origin of the Australian dingo, obtained from the study of mitochondrial DNA. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[27]  J. Lundeberg,et al.  Genetic Evidence for an East Asian Origin of Domestic Dogs , 2002, Science.

[28]  Swapan Mallick,et al.  A direct characterization of human mutation based on microsatellites , 2012, Nature Genetics.

[29]  R. Durbin,et al.  Inference of human population history from individual whole-genome sequences. , 2011, Nature.

[30]  J. Lundeberg,et al.  mtDNA Data Indicate a Single Origin for Dogs South of Yangtze River, Less Than 16,300 Years Ago, from Numerous Wolves , 2009, Molecular biology and evolution.

[31]  H. Ellegren,et al.  Genes of domestic mammals augmented by backcrossing with wild ancestors. , 2005, Trends in genetics : TIG.

[32]  David Reich,et al.  Testing for ancient admixture between closely related populations. , 2011, Molecular biology and evolution.

[33]  Faraz Hach,et al.  Sensitive and fast mapping of di-base encoded reads , 2011, Bioinform..

[34]  G. Larson,et al.  A population genetics view of animal domestication. , 2013, Trends in genetics : TIG.

[35]  Jeremiah D. Degenhardt,et al.  A Simple Genetic Architecture Underlies Morphological Variation in Dogs , 2010, PLoS biology.

[36]  Jeremiah D. Degenhardt,et al.  Genome-wide SNP and haplotype analyses reveal a rich history underlying dog domestication , 2010, Nature.

[37]  A. Boyko,et al.  Linkage Disequilibrium and Demographic History of Wild and Domestic Canids , 2009, Genetics.