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Link to original content: http://pubmed.ncbi.nlm.nih.gov/39193769
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. 2024 Sep 3;16(9):evae190.
doi: 10.1093/gbe/evae190.

Comparative Population Genomics of Arctic Sled Dogs Reveals a Deep and Complex History

Tracy A Smith  1 , Krishnamoorthy Srikanth  2 , Heather Jay Huson  2
Affiliations

Comparative Population Genomics of Arctic Sled Dogs Reveals a Deep and Complex History

Tracy A Smith et al. Genome Biol Evol. .

Abstract

Recent evidence demonstrates genomic and morphological continuity in the Arctic ancestral lineage of dogs. Here, we use the Siberian Husky to investigate the genomic legacy of the northeast Eurasian Arctic lineage and model the deep population history using genome-wide single nucleotide polymorphisms. Utilizing ancient dog-calibrated molecular clocks, we found that at least two distinct lineages of Arctic dogs existed in ancient Eurasia at the end of the Pleistocene. This pushes back the origin of sled dogs in the northeast Siberian Arctic with humans likely intentionally selecting dogs to perform different functions and keeping breeding populations that overlap in time and space relatively reproductively isolated. In modern Siberian Huskies, we found significant population structure based on how they are used by humans, recent European breed introgression in about half of the dogs that participate in races, moderate levels of inbreeding, and fewer potentially harmful variants in populations under strong selection for form and function (show, sled show, and racing populations of Siberian Huskies). As the struggle to preserve unique evolutionary lineages while maintaining genetic health intensifies across pedigreed dogs, understanding the genomic history to guide policies and best practices for breed management is crucial to sustain these ancient lineages and their unique evolutionary identity.

Keywords: Arctic dogs; Siberian Husky; canine evolution; canine genetic health; sled dogs.

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Conflict of interest statement

T.A.S. has both show and racing Siberian Huskies and participates in AKC conformation and sled dog racing sports. H.J.H. has formerly participated in sled dog races with Alaskan sled dogs. K.S. declares no competing interests.

Figures

Fig. 1.
Fig. 1.
PCAs of Arctic and West Eurasian dogs. Each point represents an individual dog. Colors signify owner-reported population or breed. a) PCA of all breeds included in this study, including two projected ancient dogs (Zhokov and AL3194), using the balanced data set (n = 91). The two main principal components explain ∼29% of the observed genetic variation. b) PCA of all Siberian Husky (show, sled show, pet, racing, and Seppala populations) and Alaskan sled dogs with closely related individuals removed (kinship coefficient < 0.088; n = 218). Numbers denote the ten subsampled individuals per population used in the balanced data set. The ellipse represents the 99% confidence interval assuming a multivariate t-distribution. The two main principal components explain ∼40% of the observed genetic variation. Starting in the lower left-hand corner, images are of dogs in the show, pet, racing (firmly inside ellipse) (copyright owner Megan Moberly), Seppala (copyright owner Louise Evans), racing (outside of ellipse), and Alaskan sled dog (copyright owner Jaye Foucher) populations.
Fig. 2.
Fig. 2.
Barplot showing individual admixture proportions inferred by ADMIXTURE (Alexander et al. 2009; Alexander and Lange 2011) for select values of K using the balanced data set of ten dogs per population (five for CSD and nine for Greenland) with closely related individuals removed (kinship < 0.088). Each vertical bar represents an individual dog. Colors represent assignment to K source populations. The ancient precontact dog AL3194 clusters with Alaskan and Greenland sled dogs. The ancient Zhokhov dog shares most of its ancestry with Alaskan and Greenland sled dogs and also shares 22% of its ancestry with modern Siberian dogs in K = 8. Pet, racing, Seppala, show, and sled show are populations within the Siberian Husky breed. Barplot was visualized in StructuRly v.0.1.0 (Criscuolo and Angelini 2020).
Fig. 3.
Fig. 3.
Evolutionary relationships and admixture modeling in the Siberian Husky and other breeds. a) Cladogram showing the phylogenetic relationships between dogs in the balanced data set inferred using a GTR model and the approximately maximum-likelihood method in FastTree v2.1.11 (Geneious version 2023.0.4; available from https://www.geneious.com). Ancient Yana wolf was used to root the tree. Bootstrap support values are shown above the branches. b) Admixture graph inferring the demographic history using qpGraph in ADMIXTOOLS v2.0.0 (Patterson et al. 2012). Dotted lines and percentages reflect admixture events and ancestry proportions. Branch lengths and numbers denote genetic drift units (f2 statistics) multiplied by 1,000. The best-fitting model shown here is the one with the lowest (negative) likelihood score (6.85) and worst residual z-score (WR = 1.08) with eight admixture events. c) The European ancestry proportions (alpha) are shown as points and were computed using the ratio of f4(GSP:Wolf; X:Greenland)/f4(GSP:Wolf; GSD:Greenland). Vertical and horizontal lines denote three standard errors. Golden Retriever, a European breed, was included as a positive control. An absolute Z-score ≥ 3 was considered significant and are shown in color (gray is not significant).
Fig. 4.
Fig. 4.
Individual D-statistics showing West Eurasian introgression in the Arctic breeds. A) A summary of D-statistics for the first ten individuals per population using (((Greenland3, Arctic Dog) European) Wolf). All dogs are shown in supplementary fig. S6, Supplementary Material online. Points show the D statistic and vertical and horizontal lines denote three standard errors. Progressively more negative D values indicate that the Arctic dog shares increasingly more derived alleles with the European breed, which signifies introgression. Absolute Z-scores ≥ 3 were considered significant (|Z| ≥ 3) and are shown in color whereas values < 3 are shown in gray and are not significant. B) A summary of West Eurasian introgression by population as determined by D statistics across all dogs in supplementary fig. S6, Supplementary Material online. Numbers represent the number of individual dogs showing significant introgression (|Z| ≥ 3) with that European breed.
Fig. 5.
Fig. 5.
Fossil calibrated divergence time estimates and admixture modeling. a) A time-calibrated MCC tree using SNAPP v1.6.1 (Bryant et al. 2012), implemented in BEAST2 v2.7.5.0 (Bouckaert et al. 2014), using divergence time estimation methods of Stange et al. (2018). Labels to the right of the nodes are mean height node ages. The 95% HPD intervals for node ages are shown with gray bars. b) Admixture graph inferring demographic history using qpGraph in ADMIXTOOLS v2.0.0 (Patterson et al. 2012). Dotted lines and percentages reflect admixture events and ancestry proportions. Numbers on branches denote genetic drift/selection units (f2 statistics) multiplied by 1,000. The best-fitting model shown here has three admixture events with a score of 3.61 and WR = 1.16 and shows substantial ancient wolf ancestry in the Zhokhov/Greenland lineage. c) Pleistocene wolf introgression is also evident in the Greenland sled dog/Zhokhov lineage using TreeMix (Pickrell and Pritchard 2012) and is not found in other Arctic dog breeds. Residuals above 0 indicate the two breeds are more closely related than illustrated by the tree and thus may be admixed. d) A predicted phenotypic reconstruction of the ancient Zhokhov sled dog based on genotypes at various coat color and other trait loci (supplementary table S10, Supplementary Material online).
Fig. 6.
Fig. 6.
Summary of the genetic health across populations of the Siberian Husky and other Arctic breeds. Asterisks represent a significant difference between populations using the Wilcoxon test. Show, racing, Seppala, and pet are populations of the Siberian Husky. a) Effective population size (Ne) over time estimated from LD in modern Arctic breeds. The Seppala Siberian and Malamute have the lowest Ne today at 47 and 41, respectively. b) Boxplot distribution of FROH across Siberian Husky populations and other Arctic breeds. Horizontal lines represent the median, vertical lines represent the range, larger circles represent the mean, and dots represent outliers. The pet and racing FROH are not significantly different. c) Distribution of the frequency of mutated evolutionarily constrained positions (PhyloP FDR < 0.05) in the Siberian Husky. d) Distribution of the frequency of deleterious mutations in the Siberian Husky.
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