Arctic-adapted dogs emerged at the Pleistocene-Holocene transition

Abstract

Although sled dogs are one of the most specialized groups of dogs, their origin and evolution has received much less attention than many other dog groups. We applied a genomic approach to investigate their spatiotemporal emergence by sequencing the genomes of 10 modern Greenland sled dogs, an ~9500-year-old Siberian dog associated with archaeological evidence for sled technology, and an ~33,000-year-old Siberian wolf. We found noteworthy genetic similarity between the ancient dog and modern sled dogs. We detected gene flow from Pleistocene Siberian wolves, but not modern American wolves, to present-day sled dogs. The results indicate that the major ancestry of modern sled dogs traces back to Siberia, where sled dog-specific haplotypes of genes that potentially relate to Arctic adaptation were established by 9500 years ago.

Fig. 1. Geographic location of the samples and overall genetic affinities.

(A) Identity by State pairwise distances between Zhokhov and present-day dogs (Table S1), geographic affiliation of dogs and archaeological sites. Color scale indicates genetic distance between Zhokhov and each sample. Circles and triangles represent modern and ancient dogs, respectively. Stars show Zhokhov and Yana sites. (B) Principal Component Analysis using whole-genome data (2,200,623 transversion sites) on all samples. (C) Treemix admixture graph built using whole genome data (766,082 transversion sites) on a dataset consisting of 66 canids merged into 15 groups according to their geographic location and admixture profile (Table S1 and Fig. S6). Colors indicate main groups as in panel B. Arrows show inferred admixture edges colored by migration weight. (D) D-statistic of the form D(H1, Boxer dog; Taimyr/Yana, Andean fox) testing for Pleistocene wolf gene flow in ancient and modern dogs, testing whether samples share more alleles with Taimyr (x-axis) or Yana (y-axis) wolves when compared to the boxer dog. Color indicates the type of sample in H1. Points show the D-statistic, while horizontal and vertical lines show 3 standard errors for the test with the Taimyr (x-axis) and Yana (y-axis), respectively. The results obtained from both ancient wolves fall along the diagonal, suggesting they are symmetrically related to all dogs.

Fig. 2. Relationships between Zhokhov and present-day sled dogs (sled dogs).

(A) D-statistics testing the relationships between pairs of sled dogs and Zhokhov. Cell colors indicate the Z-scores obtained from the test D(dog1, dog2; Zhokhov, Andean fox), where dog1 and dog2 are all possible pairs of sled dogs. Comparisons involving pairs of Greenland sled dogs and non-Greenland sled dogs resulted in significant deviations from H0 (|Z|>3). (B) D-statistics showing that sled dogs that are significantly further from Zhokhov compared to Greenland sled dog Aasiaat 2 (y-axis: D(Greenland sled dog Aasiaat 2, H2; Zhokhov, Andean fox)) also show evidence of significant gene flow from other dogs (x-axis: D(Greenland sled dog Aasiaat 2, H2; German shepherd dog, Andean fox)). Points indicate the D-statistic, while horizontal and vertical lines indicate 3 standard errors for the x- and y-axis, respectively. We considered the test to be significant for gene-flow when these lines do not overlap with the dotted line (|Z|>3).

Fig. 3. Adaptation.

(A) Manhattan plot of the PBS values (y-axis) in windows of 100 kilo-base pairs (kb) using a 20 kb slide across chromosomes (x-axis). Data points between the 20^th and 80^th percentile of the empirical distribution are not plotted and dashed red lines show the 99.95^th and 0.05^th percentiles. Names of genes within the highest peaks are shown, with asterisks representing no overlap with genes. We note that other genes not displayed in the figure can overlap the outlier regions, a full list can be found in Table S4-5. Haplotype structures for TRPC4 (B), CACNA1A(C) and MGAM (D). Rows represent individuals, columns polymorphic positions in the dog genome. Cells are colored by genotype: dark gray (alternative allele homozygous), light gray (heterozygous) and white (reference allele homozygous). The row height for ancient individuals was increased to facilitate visualization. Zhokhov is highlighted with a red asterisk. SDs is used as an acronym for sled dogs.