The Journal of Heredity 2001:92(5)
© 2001 The American Genetic Association 92:398-403
Genetic Variability in East Asian Dogs Using Microsatellite Loci Analysis
From the Department of Genetic Engineering, College of Natural Sciences, Kyungpook National University, 1370 Sankyuk-dong, Puk-gu, Taegu 702-701, Korea (Kim and Ha), Department of Animal Science and Technology, Azabu University School of Veterinary Medicine, Fuchinobe, Kakamigahara, Japan (Tanabe), and Department of Biological Sciences, Korea Advanced Institute of Science and Technology, Taejon 305-701, Korea (Park).
Address correspondence to Ji-Hong Ha at the address above or e-mail: jhha{at}bh.kyungpook.ac.kr.
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Abstract |
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An analysis of eight microsatellite loci in 213 animals was performed to define the genetic structure and variability of 11 East Asian native dog populations. Allele diversity, observed heterozygosities, expected heterozygosities, F-statistics, GST estimates, number of migrants per generation (Nm), and Nei's DA distance were calculated. Expected mean heterozygosities of Asian native dogs varied within a range of 0.310–0.718 with a mean value of 0.580. In a sample of 11 Asian dogs, the highest genetic diversity was exhibited in the Korean native dogs and the lowest in the Shiba, the Japanese native dog. All populations except the Kishu and Akita showed statistically significant deviation from Hardy–Weinberg equilibrium at more than one locus. After corrections for multiple significance tests, deviations over all loci were statistically significant in 7 of 11 dog populations, meaning that Asian dogs are genetically subdivided (global FST = 0.154). Despite the locus-specific deviations, statistically significant departures from the Hardy–Weinberg equilibrium reflect deviations in the direction of heterozygote deficit, the global FIS being 0.072. In the neighbor-joining and unweighted pair group method with arithmetic mean (UPGMA) dendrograms based on Nei's DA distance, the Korean native breeds (the Sapsaree and the Jindo) were grouped together, then with the Eskimo dog. The two Japanese native dogs (the Hokkaido and the Akita) also clustered together, with moderate bootstrap support. In spite of some deviation, the three-dimensional scattergram based on principal components supported the conclusions suggested by the dendrograms based on Nei's DA distance. From these two analyses, the Korean native dogs formed the closest groups and then showed a close relationship to the Eskimo dogs, reflecting the fact that the Korean native dogs might be originated from dogs in the northern part of Far East Asia.
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Introduction |
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The dog (Canis familiaris), which was domesticated from the wolf in the preagricultural age (Roy et al. 1994; Tanabe 1991; Turnbell and Reed 1974), has been well characterized as including more than 400 breeds with various morphological and behavioral traits. However, there have been few studies on the genetic backgrounds and genetic polymorphisms between these breeds (Fredholm and Wintero 1995; Koskinen and Bredbacka 2000; Zajc et al. 1997).
Most of the research has been performed on European dog breeds. An extensive genetic relationship study among Asian dog breeds was conducted using the allozyme polymorphism of blood protein (Tanabe et al. 1991). However, since allozyme loci have low mutation rates of 
10-8/generation (Nei 1987), few detectable sequence substitutions of closely related dog populations would have been accumulated in the allozyme loci.
Microsatellites display higher levels of variation, and consequently enable more efficient finding of population differentiation than allozymes. Microsatellites are repetitive DNA sequences that are randomly distributed throughout eukaryotic genomes. Microsatellite loci are highly polymorphic with high mutation rates of more than 10-4 per generation and are abundant in the eukaryotic genome having 50,000–100,000 loci (Litt and Luty 1989). Although the dog has diverged recently and maintained a relatively low genetic variability due to artificial selection and inbreeding, canine microsatellites have been successfully utilized in the population genetics of the Canidae family (Fredholm and Wintero 1995; Koskinen and Bredbacka 2000; Roy et al. 1994; Zajc et al. 1997). Until now, dendrograms based on genetic distances calculated from gene frequencies have been commonly used to explain the genetic relationships among animal populations. However, dog phylogeny is still a challenging problem largely because the origin of any given breed can be complex, involving multiple ancestral types.
In Asia, many dog breeds occupy highly restricted, allopatric ranges. Asian local native peoples have inbred native dog breeds without any crossbreeding with other dogs to maintain their pedigree and their specific physical characteristics. Therefore Asian native dog breeds are good resources for subdivision and diversity studies of dog populations.
Here we investigated the genetic variability and population structures of 11 East Asian native dog breeds and populations using eight microsatellites and determined the genetic relationship between them using two analytical methods—Nei's genetic distance formula and a principal component analysis. We also speculate on the origin and migration route of Korean native dogs from the genetic relationships among Asian native dogs.
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Materials and Methods |
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Dog Samples and Description of Native Dog Breeds in East Asia
Blood samples were collected from the foreleg vein of 213 individual dogs from 11 Asian native dog populations, including eight dog breeds. The sampled numbers, breeds, and populations were as follows: three Korean native dogs (Sapsaree, n = 30; Jindo, n = 21; heterogeneous aboriginal dog (HAD) population, n = 15), four Japanese native dogs (Shiba, n = 20; Akita, n = 22; Kishu, n = 21; Hokkaido, n = 21), one arctic dog (Eskimo dog, n = 21), one Chinese origin breed (Shih Tzu, n = 11), one Sakhalin native dog, n = 15, and the Taiwanese dog population, n = 16). Fresh blood was taken from individuals from well-defined geographical areas and chosen at random without consideration of the relationship between breeds. The geographical locations of the dog populations in Korea and adjacent areas used in this study are given in Figure 1. Of these dogs, the Korean native aboriginal dogs (HADs), the Sakhalin, and the Taiwanese native dogs are not breeds. Blood samples from them were sampled randomly from several areas in Korea, the Sakhalin, and the mountain area of Taiwan Island, respectively.
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The Jindo and the Sapsaree are registered as Korean native breeds. The Jindo is a medium-sized breed (body height 47–55 cm) originating on Jindo Island and spreading all over Korea. We took blood samples from pedigreed dogs on Jindo Island. The Sapsaree is a long-haired, medium-sized breed (body height 49–55 cm) originating in the Kyungpook provinces. The Sapsaree has been conserved in a restricted area, Kyungsan, exempting it from endangered status. The Hokkaido dog, a Japanese native dog, is a medium-sized breed (body height 40–55 cm) originating on Hokkaido Island. It was once called the Ainu dog because it was kept by Ainu. The Akita is a large breed (body height 58–70 cm) originating in Akita Prefecture. The Kishu is a medium-sized breed (body height 46–55 cm) originating in Wakayama Prefecture. The Shiba is a small breed (body height 35–41 cm) consisting of four local varieties, of which Shinshu Shiba, originating in Nagano Prefecture, is the major variety, spreading all over Japan. A powerfully built, medium-sized native of the arctic, the Eskimo dog, is prized for its stamina and vigor. We took blood samples of the Eskimo dogs (pedigreed) in the Obihiro Zoo and adjacent areas. The blood samples from the Chinese dog breed, the Shih Tzu (pedigreed), were collected from various institutions and veterinary hospitals in Japan.
DNA Extraction and Microsatellite Analysis
Genomic DNA was extracted from the ACD stabilized blood samples of all of the dogs as described by Sambrook et al. (1989). Eight unlinked microsatellite loci from the domestic dog genomic library (Francisco et al. 1996) were used for the analysis of the Asian native dogs. A polymerase chain reaction (PCR) analysis was carried out by 5' end-labeling one primer of each primer set with a standard [
-32P]ATP using T4 polynucleotide kinase (Promega). The PCR reaction was accomplished in a total volume of 12.5 µl using 25 ng of genomic DNA, 2.0 mM of MgCl2, 200 µM of each dNTP, 4 pmol of each primer, and 0.5 unit of Taq polymerase. The reaction cycle was accomplished by denaturation for 1 min at 94°C, primer annealing for 45 s at the desired temperature, and an extension for 1 min at 72°C and repeated 28 times. Three microliters of the amplified product was then mixed with an equal volume of formamide loading dye and heated to 95°C for 3 min. Three microliters of the mixed product were separated on a 6% polyacrylamide gel and autoradiographed for 6–12 h. The discrimination of the microsatellite alleles was determined by comparison with an adjacent DNA sequencing ladder.
Genetic Analysis
Allele frequencies (available from the authors upon request), the mean number of alleles per locus, observed heterozygosity (Ho), and heterozygosity expected from Hardy–Weinberg assumptions (He) for each locus were computed using the GENETIX software package (Belkhir et al. 1996–1998). The two measures of heterozygosity are highly correlated; however, this study focused on the expected heterozygosity, since it is considered to be a better estimator of the genetic variability present in a population (Nei 1987). The GENETIX program was further used to calculate GST, an estimator of genetic differentiation, and indirect estimates of gene flow, the number of migrants per generation (Nm) (Wright 1969). The GENEPOP version 3.1b program (Raymond and Rousset 1995) was employed to test deviations from the Hardy–Weinberg equilibrium and to assign FIS, FIT, and FST estimates (Weir and Cockerham 1984). For the Hardy–Weinberg equilibrium estimation, we followed the probability test approach (Guo and Thomson 1992). To know whether the deviations from Hardy–Weinberg equilibrium were in the direction of heterozygote excess or deficit, Hardy–Weinberg tests for each locus in each population and a global test over all populations were performed. Corrections for multiple significance tests were performed using Fisher's method and by applying a sequential Bonferroni correction (Rice 1989). FIS estimates were calculated across all populations and loci (global FIS), and for populations and loci individually. Similarly the FST calculations were performed over all populations (global FST), and all combinations formed by two populations were addressed individually (pairwise FST).
The genetic relationships among Asian dogs based on allele frequencies at microsatellite loci were analyzed using two different approaches. First, genetic divergence between the breeds was calculated according to DA genetic distance (Nei et al. 1983) using the DISPAN computer program (Ota 1993). Phylogenetic trees were constructed using neighbor-joining (NJ) clustering (Saitou and Nei 1987) and the unweighted pair group method with arithmetic mean (UPGMA) (Sneath and Sokal 1973) from DA distance. Bootstrap resampling (n = 1000) was performed to test the robustness of the dendrogram topologies. As an alternative approach to represent the genetic relationship among the dog breeds, a principal component analysis (PCA) was also applied using gene frequencies of all the variable loci. The frequencies of all the alleles at a single locus were considered as independent variables, even though they were not independent from each other as their sum is unity. Accordingly, correlation matrices were computed from the gene frequencies of all the loci, as well as the eigenvalues of all the principal components, the proportions of individual eigenvalues to the total variance (contribution rates of components), and the raw scores of every dog for each of the principal components. A scattergram of the score data was examined to visualize the geometric relationships among the Asian dogs. PCA using microsatellite data was performed using the XLSTAT program (Agresti 1990; Saporta 1991).
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Results |
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Genetic Variability in Asian Native Dogs
The allele and genotype frequencies of eight microsatellite loci were determined in 11 Asian native dog breeds and populations (details available from the authors). The eight dog microsatellite markers used in this study showed reproducible and discernible bands. Although some unique alleles were found in certain populations, these are unlikely to be useful as breed markers due to their low frequency in a small sample size. The mean number of alleles per locus and the observed and expected heterozygosities averaged over all the microsatellite loci in each dog breed and population are shown in Table 1. For the eight microsatellites, the number of alleles per locus ranged from 2.63 (the Shiba) to 5.88 (the Jindo) with a mean of 4.34. Observed and expected mean heterozygosities for the different dog breeds ranged from 0.275 to 0.717 and 0.310 to 0.718, respectively. Over all populations, from 4 (CXX.2060) to 12 (CXX.2004) alleles per locus were observed (Table 2).
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From 88 instances (11 populations, 8 loci), 19 deviations significant at the 5% level from Hardy–Weinberg equilibrium were detected (Tables 1 and 2). All populations except the Kishu and the Akita showed significant deviation from Hardy–Weinberg equilibrium at more than one locus. Three of these deviations were negative and 16 positive FIS values. After corrections for multiple significance tests, deviations over all loci were significant in 7 of 11 dog populations. Over all populations and loci, Hardy–Weinberg disequilibrium was statistically highly significant (Table 1).
At individual loci, FIS estimates over all dog populations ranged between -0.0914 (the locus CXX.2062) and 0.3426 (the locus CXX.2050), the global FIS being 0.072 (Table 2). Despite these locus-specific deviations, statistically significant departures from the Hardy–Weinberg equilibrium reflect the deviation in the direction of heterozygote deficit.
The different estimates of genetic differentiation (FST and GST) with the FIS and FIT are shown in Table 2. The FST and GST values for each locus are very close and levels of apparent breed differentiation were considerable. Multilocus FST values indicate that approximately 15.4% of the total genetic variation was explained by breed differences, with the remaining 84.6% corresponding to differences among individuals. Genetic differentiation among breeds was highly significant (P < .01) for all loci. On average, breeds had a 7.2% deficit of heterozygotes, whereas the total population had a 20.6% deficit of heterozygotes.
Genetic Relationships Among the Asian Native Dogs
Table 3 presents Nei's DA distance, FST, and Nm values when breeds are considered in couples. Across the eight loci, the mean genic differentiation values (FST) ranged from 2.3% for the Taiwanese-Sakhalin dog pair to 37% for the Shiba-Hokkaido dog pair (Table 3). The number of migrants per generation (Nm) varied from 10.83 for the Taiwanese-Sakhalin dog pair to 0.43 for the Shiba-Hokkaido dog pair, indicating high gene flow between the Taiwanese and the Sakhalin dogs. It is noted that gene flow among the Korean native dogs is relatively high compared with other dog breeds. The smallest DA distance (0.084) was observed between the Sapsaree and Jindo dog, and the largest (0.324) between the Shiba and the HAD.
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Relationship trees among 11 Asian native dog breeds and populations were constructed based on Nei's DA distance matrix (Figure 2). In the neighbor-joining and UPGMA dendrograms, apart from HAD, the Korean native dogs (the Sapsaree and Jindo) were grouped together, and the two Japanese native dogs (the Hokkaido and Akita) also clustered together, with moderate bootstrap support. Two of the four Japanese breeds, the Shiba and Kishu, formed the basal branch for all other dogs, including the Korean and the Chinese native dogs. These relationships are difficult to understand in relation to the geographical areas of distribution and origins of the breeds.
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In order to further understand the geographical relationship and complicated interrelationships among Asian native dogs, a PCA based on the correlation matrix obtained from the allele frequencies was also performed. The standardized scores for the first (axis 1), second (axis 2), and third (axis 3) principal components for each of the 11 Asian dog breeds and populations are given in Table 4. In the case of the first principal component, the Korean and Sakhalin dogs had a very high minus value (direction), whereas some of the Japanese, the Chinese, and the Taiwanese dogs had a plus value (direction). Of Asian dogs studied, the Shiba exhibited the largest plus value (direction). In the case of the second principal component, the three Japanese dogs, except for the Shiba, showed a high minus value (direction). In terms of the principal component values, the Korean dogs showed similar relationships, exhibiting relatively similar directions and values, whereas the Japanese dogs were scattered in a variety of distributions.
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To more easily understand the geographic relationships among Asian dogs, the standardized values for axis 1, 2, and 3 were plotted on a three-dimensional scattergram (Figure 3). These three components account for 46% of the total variance. In the scattergram, the Korean native and Eskimo dog breeds exhibited a close relationship, forming the same group, whereas the three Japanese dogs, except for the Shiba, formed similar groups with a large distribution. Also, the Taiwanese dog and the Chinese dog, the Shih Tzu, exhibited a close group. In spite of the difference in the relationship between the Taiwanese and Sakhalin dogs, the three-dimensional scattergram supported the conclusions suggested by the dendrograms based on Nei's DA distance. From these two analyses, the Korean native dog breeds formed the closest groups, showing a close relationship to the Eskimo dogs.
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Discussion |
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The task of resolving the genetic relationships of domestic dog breeds is a very difficult one given the varied origins of and substantial gene flow among breeds. According to previous studies (Okumura et al. 1996; Tsuda et al. 1997), frequency differences in nuclear markers may be the best hope for resolving the relationships of breeds. In this study we investigated the allele frequencies and genotype distributions of eight microsatellite loci in 213 individuals of East Asian native dogs. In this study, after corrections for multiple significance tests, 7 of 11 dog populations showed significant deviations over all loci. In addition, Hardy–Weinberg disequilibrium was statistically highly significant over all populations and loci, showing a departure from the Hardy–Weinberg equilibrium in the direction of heterozygote deficit. These results mean that Asian dogs are genetically subdivided (global FST = 0.154). Given the breeding practices in the dog world (selection and inbreeding effects), Hardy–Weinberg equilibrium is likely to be the exception rather than the norm. Also, considering the high genetic homogeneity in domestic dogs, a certain degree of nonconformity to Hardy–Weinberg equilibrium is expected (Zajc et al. 1997).
In our study, allele nonamplification is unlikely to have contributed significantly to the deviation from Hardy–Weinberg equilibrium. When tested in large reference dog pedigrees, all microsatellites used in this study showed true Mendelian inheritance and null alleles were not detected. The main reasons for the deviation from Hardy–Weinberg equilibrium are most likely the limited sample size, extensive gene flow, or nonrandom mating of purebred dogs. Especially for the Eskimo dog, six of eight loci showed highly significant deviation (P < .01) from Hardy–Weinberg equilibrium (Table 1). Deviation from Hardy–Weinberg equilibrium is probably related to the sampling procedures, as samples were mainly collected in the zoo-kept animals.
The microsatellite loci showed a high variability in Asian dogs with 4–12 alleles/loci and mean heterozygosities ranged from 0.310 (Shiba) to 0.718 (HAD). Although different markers were used, the expected mean heterozygosities of Asian dogs are similar to those of European dogs (0.56, Bedlington terriers; 0.62, golden retriever; 0.64, Pembroke Welsh corgi; 0.64, German shepherd; and 0.72, wirehaired dachshund) (Koskinen and Bredbacka 2000). Of Asian dogs, the Korean native dogs, including the Sapsaree, Jindo, and HAD, showed a relatively higher polymorphism. In contrast, the Japanese native dogs exhibited low genetic variability among breeds and populations (mean expected heterozygosity 
0.5), reflecting low intrabreed variation and extensive inbreeding. Furthermore, the Shiba had the smallest average allele number as well as the lowest heterozygosity (0.310), showing a considerable reduction in intrabreed variation. It is assumed that the Shiba has been maintained separately without any interbreeding with other dogs due to the small physical size of its breed.
The relationship between man and dog can be called a partnership, but not the commensalism that is usually observed between man and other domesticated animals (Zeuner 1963). Dogs have migrated with man since ancient times. Because the migration of man bears a close relationship to the migration of dogs, tracing the migration routes of dog populations is one way to trace the migration routes of prehistoric man. Accordingly, a relationship study among Asian native dogs may provide an important clue to understanding the origin and migration of Asian people in the prehistoric age. Tanabe et al. (1991) proposed the migration of the Japanese people based on the polymorphism of blood protein loci. They suggested that there were at least two waves of gene flow for dogs into Japan: the first was from Southeast Asia to all the Japanese islands; the second was from the Korean peninsula to the main Japanese islands. The relationship trees based on Nei's DA distance and the three-dimensional scattergram based on the principal components show that Japanese dogs have a high genetic variety among their native dogs, with relatively heterogeneous gene constitutions. The genetic variety of Japanese native dogs suggests that the dogs may consist of populations derived from several genetically different ancestral populations and their crossbreeds rather than from a single origin. Both analyses indicate that Korean native dogs form a closely related group, showing a close relationship to Eskimo dogs. It is interesting that the close relationship observed between Korean native dogs and Eskimo dogs may reflect the migration of the Scythian people from central North Asia to East Asia in the prehistoric age. Some researchers (Ha and Kim 1998; Tanabe 1991) suggest that Korean native dogs originated from dogs in the northern part of Far East Asia. However, for that conclusion, the larger dog populations from central and northeast Asia, including China, Mongolia, and Siberia need to be examined.
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Acknowledgments |
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We would like to thank two anonymous reviewers for helpful discussions and comments on the manuscript. This research was supported by the Korea Science and Engineering Foundation, and by the Creative Research Initiative Program.
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Footnotes |
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Corresponding Editor: Stephen J. O'Brien
Received March 6, 2000
Accepted June 30, 2001
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References |
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