Population structure and genetic history of Tibetan Terriers

Abstract

Background: Tibetan Terrier is a popular medium-sized companion dog breed. According to the history of the breed, the western population of Tibetan Terriers includes two lineages, Lamleh and Luneville. These two lineages derive from a small number of founder animals from the native Tibetan Terrier population, which were brought to Europe in the 1920s. For almost a century, the western population of Tibetan Terriers and the native population in Tibet were reproductively isolated. In this study, we analysed the structure of the western population of Tibetan Terriers, the original native population from Tibet and of different crosses between these two populations. We also examined the genetic relationships of Tibetan Terriers with other dog breeds, especially terriers and some Asian breeds, and the within-breed structure of both Tibetan Terrier populations.

Results: Our analyses were based on high-density single nucleotide polymorphism (SNP) array (Illumina HD Canine 170 K) and microsatellite (18 loci) genotypes of 64 Tibetan Terriers belonging to different populations and lineages. For the comparative analysis, we used 348 publicly available SNP array genotypes of dogs from other breeds. We found that the western population of Tibetan Terriers and the native Tibetan Terriers clustered together with other Asian dog breeds, whereas all other terrier breeds were grouped into a separate group. We were also able to differentiate the western Tibetan Terrier lineages (Lamleh and Luneville) from the native Tibetan Terrier population.

Conclusions: Our results reveal the relationships between the western and native populations of Tibetan Terriers and support the hypothesis that Tibetan Terrier belongs to the group of ancient dog breeds of Asian origin, which are close to the ancestors of the modern dog that were involved in the early domestication process. Thus, we were able to reject the initial hypothesis that Tibetan Terriers belong to the group of terrier breeds. The existence of this native population of Tibetan Terriers at its original location represents an exceptional and valuable genetic resource.

Fig. 1

Relationship of Tibetan Terriers with other dog breeds. Neighbor-joining tree based on SNP chip data for 161 dog breeds revealing a compact cluster of ancient dog breeds including native Tibetan Terrier and F1 crosses with its western lineages. The western lineages are part of the Tibetan Companion Dog cluster

Fig. 2

NeighborNet network relating 27 dog breeds and Grey Wolf. NeighborNet network, based on Nei’s genetic distances, reveals the relationships between 27 dog breeds and Grey Wolf. Reticulations on the graph indicate past hybridization events between populations. Breed names are abbreviated as follows: Airedale Terrier (AIR), American Pit Bull Terrier (APB), American Staffordshire Terrier (AST), Bedlington Terrier (BET), Border Terrier (BORT), Boston Terrier (BOST), Bull Terrier (BullT), Cairn Terrier (CT), Fox Terrier Wire (FTD), Jack Russell Terrier (JRT), Japanese Chin (Chin), Kerry Blue Terrier (KBT), Lhasa Apso (LHAP), Norfolk Terrier (NFT), Norwich Terrier (NWT), Pekingese (PEKE), Rat Terrier (RATT), Scottish Terrier (SCT), Shih Tzu (SHI), Silky Terrier (SILT), Soft Coated Wheaten Terrier (SCWT), Staffordshire Bull Terrier (SBT), Tibetan Spaniel (TIBS), Native Tibetan Terrier (TTNA), Tibetan Terrier (TT), Toy Fox Terrier (TFT), West Highland White Terrier (WHWT), Yorkshire Terrier (YOR)

Fig. 3

Migrations within the Asian toy dog and Terrier breeds. Maximum likelihood tree showing the most important migrations within the Asian toy dog- (Tibetan Terrier, Japanese Chin, Shih Tzu, Lhasa Apso, Pekingese, and Tibetan Spaniel) and Terrier breeds

Fig. 4

Genetic structure of Terriers and companion dogs. Bayesian clustering on a complete CanineHD BeadChip dataset of 29 dog breed populations and Grey Wolf (N = 366) performed with STRUCTURE and visualized using the CLUMPAK software

Fig. 5

STRUCTURE analysis of Tibetan Terrier subpopulations. STRUCTURE analysis of microsatellite (a) and SNP chip data (b) from different Tibetan Terrier subpopulations. Individuals were assigned to clusters at different K values. Breed abbreviations: TTLA: Tibetan Terrier, Lamleh lineage; TTLU: Tibetan Terrier, Luneville lineage; TTNA: Tibetan Terrier, native population; TT-F1. TT-BC2, TT-BC3: F1 and two back cross generations from the crossing of TTNA with the western TT

Fig. 6

Proportion of the autosomal genome in ROH. Proportion of the autosomal genome in ROH for 11 dog populations; considering all ROH (first panel) and ROH summarized in three length categories: short = between 0.5 and 2.5 Mb; medium = between 2.5 and 5.0 Mb; and long = more than 5 Mb