Population Structure and Genetic History of Tibetan Terriers Mateja Janeš1, Minja Zorc2, Vlatka Cubric‑Curik1, Ino Curik1 and Peter Dovc2*
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Janeš et al. Genet Sel Evol (2019) 51:79 https://doi.org/10.1186/s12711-019-0520-4 Genetics Selection Evolution RESEARCH ARTICLE Open Access Population structure and genetic history of Tibetan Terriers Mateja Janeš1, Minja Zorc2, Vlatka Cubric‑Curik1, Ino Curik1 and Peter Dovc2* 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 diferent 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 diferent 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 diferen‑ tiate 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. Background lineages were established during the history of the breed, Tibetan Terrier (TT) is a medium-sized companion dog the older Lamleh lineage, which can be traced back to the breed, which is present in many countries all over the frst two animals (Bunti and Rajah) that were acquired world. Te so-called western population of Tibetan Ter- by Dr. Agnes Greig in 1922 and brought to England in riers originated from a small number of founder animals 1930. In 1937, the Kennel Club of England recognized that were imported from the border region between the Tibetan Terrier as an own breed, based on animals Tibet and India (Central Himalaya) at the beginning belonging to the Lamleh lineage. Te second lineage of the twentieth century [1]. In western countries, two of Tibetan Terriers i.e. Luneville was formed by mat- ing Dusky, a stray dog, found by John Downey in Liver- pool in 1953 (it was registered as a Tibetan Terrier and *Correspondence: [email protected]‑lj.si named Trojan Kynos) and the bitch Princess Aureus [2] 2 Department of Animal Science, University of Ljubljana, Biotechnical (see Additional fle 1: Figure S1). Both lineages go back Faculty, Ljubljana, Slovenia Full list of author information is available at the end of the article to a very limited number of founders from the native © The Author(s) 2019. This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creat iveco mmons .org/licen ses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creat iveco mmons .org/publi cdoma in/ zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Janeš et al. Genet Sel Evol (2019) 51:79 Page 2 of 12 Tibetan Terrier (TTNA) population and represent the haplotypes across the entire canine genome and clari- link between the western population of Tibetan Terri- fed the nature of the genetic diversity within and across ers and the original population in Tibet, which supports breeds. An SNP-based analysis identifed 51 regions in the genetic relationship between both populations. How- the dog genome that are associated with phenotypic vari- ever, following recognition of the western population of ation of 57 traits [12]. An analysis of 509 dogs from 46 Tibetan Terriers by kennel clubs in Europe, the United breeds revealed 44 genomic regions, which are associated States, Australia and other countries, their population with phenotypic traits that vary between breeds [13]. underwent a long and relative strict isolation from the Recently, by investigating the genetic background of vil- original native population of Tibetan Terriers in Tibet. lage dogs, Shannon et al. [14] reported the existence of Tis isolation was broken only sporadically through a a Central Asian domestication origin and identifed geo- few imports of single animals, which refreshed tempo- graphic isolation, migration, and hybridization as impor- rarily the western population. Consequently, a very spe- tant factors that shape the genetic diversity of village cial situation was created for the western population of dog populations [14]. A genome-wide haplotype sharing Tibetan Terriers, which is a pedigree-controlled popula- analysis uncovered the geographic patterns of develop- tion that exists in parallel to the original native popula- ment and the independent origins of common traits in tion in Tibet. It is only very recently that a reproductive dogs [15]. Results based on genome-wide SNP genotypes contact between both populations occurred through a are supported by those from whole-genome sequencing, limited number of imported dogs from Tibet to the west- which has recently become a powerful approach for asso- ern countries. Te western population of Tibetan Terriers ciation studies [4, 16] and for the study of traits related to is registered at Te International Cynological Organisa- adaptation [17, 18] and dog domestication [19, 20]. With tion [Fédération Cynologique Internationale (FCI), Breed the accumulation of genomic data, evolutionary and standard N° 209, 2017]. Te original native population of functional analyses on a fner scale can be carried out. Tibetan Terriers is still present in Tibet and represents Analysis of copy number variations (CNV) has also been the original gene pool from which only a few individu- used to detect genomic regions in the dog genome that als contributed as founders to the western population of are responsible for breed-specifc phenotypes [21]. Tibetan Terriers. In addition, the native population of Te positioning of Tibetan Terriers within the terrier Tibetan Terriers contributed also to the formation of the group of dogs, which was based on a superfcial pheno- gene pool of several other Tibetan dog breeds, i.e. Lhasa typic judgement of some cynologists in the early period Apso, Shih Tzu, and Tibetan Spaniel, which are consid- of the formation of the breed, is often questioned today ered as ancient dog breeds. Tus, the native population [2]. Neither historical nor genetic data support this of Tibetan Terriers can be assigned to a limited group of decision. According to Ostrander [22], most of the ter- the early canine foundation stock [3]. rier breeds fall within the “modern/hunting” cluster of During the last two decades, a number of studies used dog breeds, which were all established from the same diferent types of genetic markers to assess the genetic pool of ancestors in Europe in the nineteenth century. variation, heterozygosity and phylogenetic relationships A few terrier breeds are found in the “mastif” cluster, between dog breeds [4]. In addition to the analysis of together with the Pomeranian and Labrador Retriever autosomal genomic regions, some studies also focused breeds. However, Tibetan Terriers cluster into the much on the Y chromosome [5] and mitochondrial DNA older group of Asian and African dogs, along with the (mtDNA) [6]. Te frst evidence on the genetic struc- Pekingese breed [22]. Furthermore, some studies classify ture of dog populations and their phylogeny and on the Tibetan Terriers into the group of ancient dog breeds [9], genetic distances between breeds emerged from stud- which is also known as the basal lineages [23]. A recent ies based on microsatellite markers (STR) [7–9], which genome-wide analysis of Korean dogs [24] examined the separated several of the breeds with an ancient origin genetic variation within Korean dog populations and from the breeds with a modern European origin. Te their relationships with wolves and ancient and modern Tibetan Terrier breed was positioned into the group of dog breeds. Among all the pairwise comparisons, the ancient Asian breeds, close to the grey wolf. STR analysis estimated FST value was highest (0.35) in the comparison can also be used to estimate population parameters and between Tibetan Terriers and the Korean wolf and thus detect population events such as past bottlenecks [10].