The origin of dog domestication and dog breeds of Japan

The dog was found to have been domesticated in East Asia (it may have been domesticated more than once, see Grimm D., likely in the south, then spreading early to nearby Japan, and then to the rest of the world. (Grimm: “Researchers report that genetic analysis of hundreds of canines—including a nearly 5000-year-old dog unearthed on the east coast of Ireland—reveals that dogs may have been domesticated twice, once in Asia and once in Europe or the Near East, although European ancestry has mostly vanished from today’s dogs. The findings could resolve a rift that has roiled the canine origins community—but experts say a lot more work needs to be done to confirm them. Source: Grimm D.,  Dogs may have been domesticated more than once Science  03 Jun 2016: Vol. 352, Issue 6290, pp. 1153-1154 DOI: 10.1126/science.352.6290.115 )

Early dog burials are known from the Jomon period, but the earliest complete (but unburied) remains are known from the Cis-Baikal region, Siberia, (earliest from Ust-Khaita dated to the Early Holocene) radiocarbon dated to 12,380 bp at the end of the Pleistocene period, and west of Cis-Baikal, another report of a 33,ooo-year-old incipient dog(-like canid) from the mountains of the Altai,

Druzhkova AS. Ancient DNA analysis affirms the canid from Altai as a primitive dog PLoS One. 2013;8(3):e57754. doi: 10.1371/journal.pone.0057754. Epub 2013 Mar 6. The analysis of 413 nucleotides of the mitochondrial control region reveal that the unique haplotype of the Altai dog is more closely related to modern dogs and prehistoric New World canids than it is to contemporary wolves.

Other dog burials reportedly the earliest are from China and Kamchatka. Canid burials first appear in the Angara River, South Baikal area around the Mesolithic-Early Neolithic transition  (Shamanka II cemetery burial with artifacts and Pad Kalashinikova, the latter dog was buried with a pebble in its mouth and Ust’ Belaia burial), see Losey RJ, Garvie-Lok S, Leonard JA, et al. Burying Dogs in Ancient Cis-Baikal, Siberia: Temporal Trends and Relationships with Human Diet and Subsistence Practices. Hart JP, ed. PLoS ONE. 2013;8(5):e63740. doi:10.1371/journal.pone.0063740.

“The Early Holocene in Cis-Baikal, referred to as the Mesolithic, is characterized by the use of microblade technologies and the absence of pottery and cemeteries (Table 1). [The inhabitants here were forager whose subsistence economies had a focus on hunting large ungulates, including deer. Faunal remains and stable carbon and nitrogen isotope values for the region’s Middle Holocene human foragers indicate that these groups relied primarily on terrestrial game such as red deer (Cervus elaphus) and roe deer (Capreolus pygargus) and increased but variable amounts of the region’s freshwater fauna, including riverine and lake fish and Lake Baikal seal (Phoca sibirica)]   One wolf burial and one unburied dog have been reported from this period [4]. Several dogs have been identified from the Early Neolithic, including burials in cemeteries [2]. Around 7000 to 6800 B.P. the Early Neolithic mortuary traditions cease–nearly no humans are interred here for ∼1000 years. At 6000 to 5800 B.P., with the advent of the Late Neolithic period, human burials again become common, but are of different mortuary traditions. Dog remains have not been reported for the Late Neolithic….

Genetic research has demonstrated that the latter human populations were genetically discontinuous with the Early Neolithic mortuary populations [6], [7]. No dog remains have been identified from the hiatus period. A third major period of forager cemetery use spans from 5200/5000 to 4000 B.P., or the Early Bronze age, and these groups may be culturally and genetically derived from local Late Neolithic populations. Dog remains previously assigned to this period include burials and isolated elements [2]. After ∼3400 B.P., pastoralists primarily herding sheep, goats, cattle, and horses arrive and establish a suite of new burial traditions [8], [9]. The chronology of Cis-Baikal’s Late Holocene culture history is subdivided here into the Late Bronze Age (∼3400 to 2250 B.P), Early Iron Age (∼2250 to 1350 B.P.), Late Iron Age (1350 to 850 B.P.), and Early Mongolian (850 to 550 B.P.) periods. No dog remains have been described from any of these periods.”

http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3145761/

The earliest dog burials in Japan date from the Jomon period 9,500 bp, see Tanabe (immediately below)

Tanabe Y., Phylogenetic studies of dogs with emphasis on Japanese and Asian breedsProc Jpn Acad Ser B Phys Biol Sci. 2007 Jan;82(10):375-87. Epub 2007 Jan 12.

Origin of Japanese dogs and their association with Japanese people

Dogs have always migrated with people. The earliest-known migrants to Japan, the Jomon people, are thought to have brought dogs to the Japanese archipelago some ten to twelve thousand years ago. The oldest dog skeletal remains discovered in Japan date from 9,500 before present (B.P.). The Jomon people, who lived by hunting and gathering, eventually settled in regions all over Japan, but mainly on Honshu, with dogs as their companions. The Jomon civilization lasted nearly ten thousand years, from 12,000 to 2,300 before present (B.P.) and through this period dogs seem to have been the sole domesticated animals. When their dogs died, their owners buried them.16)This situation of the Jomon people was similar to that of North America Amerindians at the time of the Spanish and Portuguese conquest.

The early Japanese dog was small, roughly the same size as the present-day Shiba. Furthermore, the skulls are distinguished by a long muzzle and a shallow stop (the depression in area between the eyes that connects nose and forehead) or no stop at all. It is generally believed that these early dogs of the Jomon period are the ancestor of the six Japanese breeds found today, and that the prototype of the Japanese breeds was already established in the Jomon period, which was followed by the Yayoi period, marked by fresh wave migrants (now known as the Yayoi people) to Japan from the Korean Peninsula. The Yayoi period lasted for six hundred years. Skeletal remains of dogs from the Yayoi period, unearthed in the Kuwanae burial mounds in Oita Prefecture and the Yoshinogari burial mounds in Saga Prefecture, both of which are dated roughly to two thousand years ago, show distinct differences from the Jomon period dogs. Their skulls have a prominent stop, and their frames are slightly larger than the earlier type of dog. Such evidence suggests that in the Yayoi period a new type of dog came to Japan, along with the new wave of people from the continent. The care and devotion accorded to the burial of dogs in Jomon is no longer evident in sites dating from the Yayoi period (2300–1700 B.P.). Most dog skeletons are partial and the bone are scattered; the remains show cuts and seem to have had the flesh torn off. This suggests that in the Yayoi period dogs were eaten as food, and this habit would have been unthinkable among the Jomon.16), 17)

In the years following Japan’s opening to the West in 1868, ideas about animal welfare took hold, and any lingering practices of eating dog meat disappeared almost entirely. During the late nineteenth and early twentieth centuries, all sorts of dogs were imported, particularly from Europe. In urban regions, crossbreeding between Japanese and foreign breeds proceeded rapidly, whereas in rural areas from Hokkaido to Kyushu, Japanese indigenous breeds, mainly used by hunters, were protected as local dogs and their genetic integrity preserved. In the latter half of the 1920s, amid growing national interest and pride in things Japanese, the movement to preserve Japanese dog breeds flourished. The Ministry of Education gave several Japanese dog breeds official recognition as “Natural monuments” (Protected Species): the Akita received this designation in 1931, the Kishu and Kai in 1934, the Shiba in 1936, and the Shikoku and Hokkaido in 1937. Preservation associations were established for each breed, and breed standardizations were formulated.17)

After the Second World War, thanks to the strenuous and unceasing efforts of conservation societies to restore, maintain, and preserve native breeds, Japanese dogs survived and began to flourish. One consolation in these difficult years was the fact that the indigenous breeds preserved as hunting dogs by hunters in the remote mountainous regions of Japan could be used to restore the breeds nation wide.

Apart from the six breeds above, several others should be mentioned here. One is the Chin, which was developed in Japan during the Edo period. The Chin was in fact brought to Japan from China many centuries before, and is altogether different in its morphology from other Japanese dogs, so its development does not seem to have involved any exchange of genes with indigenous Japanese dogs. There is also the Ryukyu dog, named for the subtropical island chain that arcs southwest from Kyushu. The Ryukyu dog is a breed of indigenous Japanese dog found in the Yanbaru region in the north of Okinawa Island and Ishigaki Island that followed its own separate course of development.17)

There are also the Mikawa dog of Tokushima Prefecture, and Satsuma dog of Kagoshima Prefecture, the latter of which has almost extinct. Both of these breeds have their own preservation movements, set up through the efforts of dog fancires and enthusiasts.17), 18)

Phylogenetic studies of Japanese dog breeds see this page

Significant allele frequency differences among dog groups are shown in Table II.9) Significantly higher allele frequencies of Es-2F and HbA were observed in dogs from Korea, North Sakhalin, Mongolia and Indonesia than those from China, Tai-wan, Bangladesh, West Siberia(Russia) and Europe. The relatively higher allele frequenciy of Gmog was observed in the dogs of Northeast Asia than in those of Southeast Asia, West Siberia and Europe. The frequency of Gmog was very high (0.445) in Korean dogs, low (0.140) in Japanese dogs, and very low (0.013) in Indonesian dogs. Gmog was not found in West Siberian (Russia) nor European dogs. Distribution of dog breeds and populations in and around Japan by alleles on the Gmo locus is illustrated in Fig. 3.9)

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Fig. 3.

Distribution of dog breeds in and around Japan by alleles on the Gmo (ganglioside monooxygenase). From Fig. 6 in ref. 9).

The presence of N-acetylneuramic acid (A-type) and glycolylneuramic acid (G-type) in dog erythrocyte membranes was discovered by Yamakawa’s research group.19), 20) The alleles of Gmoa and Gmog on a locus (Gmo) control the phenotypes, with the latter being found only in Japanese and East Asian dog breeds except the Hokkaido, a Japanese breed.9), 21), 22)

To clarify genetic relationships among dogs, a scattered diagram of populations of the 56 dog breeds or populations plotted on the basis of the 1st and 2nd principal component scores are illustrated in Fig. 49) (methodology reference: Tanabe et al.22)). The 1st and 2nd principal components account for 51.5%, of total variance. The figures clearly show close relationships among Mongolian, Indonesian, and North Sakhalin dogs, and among Korean and some Japanese dog breeds such as the Mikawa, the Shiba, Shikoku and the Shima lines of Mie hunting dogs. It is noteworthy that a close genetic relationship was observed between the Ryukyu living in the far south, and the Hokkaido living in the far north portion of Japan.

The first domestication of the dog occurred in East Asia, and major ancestor of the dog was a wolf subspecies, Canis lupus chanco. This finding derives from data on the nucleotide sequences of mtDNA and the frequency of genes controlling blood protein polymorphisms in various subspecies of wolves and dog breeds around the world. The results of the allele frequency distribution of genes controlling 16 blood protein polymorphisms, and the incidence of dogs possessing erythrocytes with high potassium (HK) in Japan, East Asia and Europe allowed us to posturate the following hypothesis about the origins of Japanese dogs and the history of their development. In the Jomon period the first dogs entered the Japanese archipelago from southern or northern continental Asia. These dogs eventually spread throughout Japan. Then, during the Yayoi and Kofun periods, other dogs were brought over via the Korean Peninsula, and crossbreeding occurred with the original dogs. The resulted offspring can be assumed to be the ancestors of most of the Japanese breeds that exist today. Ethological studies have revealed a significant breed difference in behavioral traits among canine breeds with Japanese dogs, showing more aggressive dispositions than most of European dogs.

In the pre-agricultural era, humans fed themselves exclusively by hunting wild animals and gathering edible plants like the wild animals, and extracting foods. Around 20,000 years ago, humans developed a symbiotic relationship with wolves for their mutual benefits. Wolves watched and guarded their residence from wild nocturnal predators animals and cooperated in humans hunting wild animals. Wolves were tamed and evolved into dogs between 15,000 and 20,000 years of age.1), 2)

Most relationships between man and the domesticated animals are modified commensalisms. Commensalism means a close association between two species of organisms, one of which is benefited by the relationship and the other is neither benefited nor harmed, but it is not a partnership, meaning that in which both are mutually benefited. The relationship between humans and dogs is mutualism. (The purpose of domestication of cats in Egypt about 4,000 years ago was to destroy parasitic mice and black rats devouring stored crops.1) The relationship of humans and cats becomes mutualism).

Wolves (Canis lupus) inhabit Eurasia and North America. There are five subspecies: Canis lupus lupus, Canis lupus chanco, Canis lupus pallipes,Canis lupus arabs and Canis lupus panbasilens. The first four inhabit Eurasia and the last one lives in northern part of North America.

Wolves have been considered to be the sole ancestor of domesticated dogs both morphologically3), 4) and ecologically.4) Canis lupus lupus, the largest inhabits Europe. Canis lupus chanco, the second largest lives in East Asia, and is currently limited to northern Asia. Canis lupus pallipes, the third largest makes its home in India and living in India and Southwest Asia. Canis lupus arabs, the smallest of the five, is native to Arabia, Israel and Syria. The last two subspecies, Canis lupus arabs and Canis lupus pallipes, especially the former were candidates for the precursors of dogs, mainly due to their smaller body size.1)

Tsuda et al.5) showed that extensive interbreeding occurred among multiple matriarchal ancestors during the domestication of dogs and a close relationship between dogs and wolves from inter-and intraspecies polymorphism in D-loop region (672-1bp) of mitochondrial DNA between dogs and wolves. Furthermore, one clade (A) containing the Chinese wolf (Canis lupus chanco) showed extensive variations while the other clade (B) showed only a slight variation (Fig. 1).

These results indicated that the ancestor of the domestic dog is the wolf, and that Canis lupus chanco was deeply involved in the domestication process of wolves. Vilá et al.6), 7) showed that the wolf was the sole ancestor of the dog from mitochondrial DNA control region sequences (261 base pair length).

Mitochondrial DNA is always inherited strictly maternally.8) Analyses of mitochondrial DNA polymorphisms and nucleotide substitutions are very useful for identifying matriarchal but not patriarchal lineages. Genetic analyses of protein polymorphisms are useful for detecting both lineages.

Tanabe et al.9) electrophoretically and chromatographically examined the allele frequencies of 16 polymorphic blood protein loci in three subspecies of wolves; Canis lupus chanco (Mongolia), Canis lupus pallipes (Afghanistan) and Canis lupus lupus (Yugoslavia), and two populations of primitive dogs,Canis familiaris hallstromi (New Guinea singing dog) and Canis familiaris dingo (Australian dingo). The mode of inheritance of the alleles on 16 polymorphic and 11 monomorphic blood protein loci is given in Table I.

Table I.

Table I.

Modes of inheritance in the 27 blood protein loci (Modified from Table I in refs. 9), 16))

From the data given in Table II, significantly higher frequencies of esterase-2F (Es-2F), ganglioside monooxygenaseg (Gmog) and hemoglobinA (HbA) were observed in Canis lupus chanco than in the other wolf subspecies.9)

Table II.

Table II.

Allele frequencies of three loci, erythrocyte ganglioside monooxygenase (Gmo), esterase-2 (Es-2) and hemoglobin (Hb) in three subspecies of wolves, New Guinea singing dog, dingo, and dog breeds and populations in Eurasia (Reconstructed from Tables 4–6

Close relationships were observed among the allele frequencies at the locus of the three loci between Canis lupus chanco and Asian dog breeds (Table II), indicating Canis lupus chanco is an ancestor of Asian dogs.

Savolainen et al.10) examined the mitochondrial DNA subsequence variation among wolves and dog populations worldwide. They established East Asian origin of the domestic dog based on a larger genetic variation in East Asia than in other regions and on the pattern of polymorphic variation.

All the data support that the first domestication of the dog occurred in East Asia, and that a major ancestor of the dog was a subspecies of wolf, Canis lupus chanco.

Migration and diversity of dogs

Dogs were domesticated in East Asia from East Asian wolves (Canis lupus chanco) more than 15,000 years ago. That date is estimated from the rate of molecular substitution of mitochondrial DNA,6), 7) and the age of ancient dog remains.2) Domesticated dogs accompanying people migrated and dispersed throughout the entire world.

It was that native American people (Amerinds) especially in North American Amerinds kept only dogs as the domesticated animal species, while the native people in South America kept dogs, and a few newly domesticated animals such as lamas, alpacas and guinea pigs. No Amerindians kept cattle, buffaloes, horses, sheep, goats, pigs or cats at the time of the Spanish and Portuguese conquest, confirming that dogs were domesticated in the pre-agricultural era.11)

Recently, mitochondrial DNA sequences isolated from ancient dog remains from Latin America and Alaska showed that American native dogs originated from old world (East Asia) lineages of dogs that were accompanied by humans in their migration across the Bering Strait in the late Pleistocene age.12)

Ancient breeds such as Canis familiaris dingo (dingoes) and Canis familiaris hallstromi (New Guinea singing dogs) were developed when human migrants and their domestic dogs reached Australia and New Guinea as early as 5,000 years ago.13)

Ancient breeds such as Canis familiaris dingo (dingoes) and Canis familiaris hallstromi (New Guinea singing dogs) were developed when human migrants and their domestic dogs reached Australia and New Guinea as early as 5,000 years ago.13)

Only one native dog breed, the Basenji, was preserved in Central Africa, and was brought to England 1895. Canine kept as hunting dogs and their ancestors were found in ancient Egypt.14)

The proposed migration routes of dogs are shown in Fig. 2.

Fig. 2.

Fig. 2.

Postulated migration routes and important locals in the domestication of the dog.

Parker et al.15) surveyed microsatellite DNA nucleotide sequences of wolves and 85 domestic dog breeds, showing that dogs could be divided into main two groups, primitive dog breeds such as Chinese (Chinese Shar-pei and Chow Chow), Japanese (Shiba and Akita), North American (Siberian, Husky and Alaskan Malamute), a native African breed (Basenji), Southwest Asian breeds (Afghan Hound and Saluki) and modern dogs including most of European breeds, which in turn can be divided into three groups: herding dog breeds appeared first, followed by hunting dogs and finally guarding dogs

The 1st and 2nd principal components account for 51.5%, of total variance. The figures clearly show close relationships among Mongolian, Indonesian, and North Sakhalin dogs, and among Korean and some Japanese dog breeds such as the Mikawa, the Shiba, Shikoku and the Shima lines of Mie hunting dogs. It is noteworthy that a close genetic relationship was observed between the Ryukyu living in the far south, and the Hokkaido living in the far north portion of Japan.

The cation composition in erythrocytes of Carnivores including dogs is high in Na and low in K (LK), because of the lack of an Na, K-pump in its cell membrane. However, some Japanese dogs possessed red blood cells with high K and low Na (HK) due to the existence of an Na, K-pump. Fujise et al.23) examined the incidence of HK and LK phenotypes of erythrocytes in dog groups from 22 breeds or population in Japan and East Asian regions adjacent to Japan (Table III). The phenotype of high K (HK) erythrocytes, which is an autosomal recessive, was found in dog groups from 10 of 13 breeds or populations in Japan. The incidence of HK was 26 to 38% in the San’in-Shiba, Shinshu-Shiba and Akita breeds, and the gene frequencies of HK ranged from 0.513 to 0.612. The highest incidence (42%) was found in the Jindo breed from Korea, with a gene frequency of 0.652. Two other groups from Korea also possessed this HK variation. HK cells were not found in dogs from Taiwan, Indonesia, Mongolia or Sakhalin. And the HK phenotype is now cleary distributed throughout Japan and Korea. The gene mutation for HK might have first occurred in Korean dogs in ancient times, and might have been subsequently distributed in Japanese dogs that accompanied humans during migrations in Yayoi and Kofun periods to Japan.

Okumura24) determined sequences of mitochondrial DNA from 145 ancient dog remains (mainly bones) from the Jomon (3,000–2,400 B.P.), the Yayoi (2,400–1,700 B.P.), the Kofun (1,700–1,400 B.P.) and the Kamakura (1,300–800 B.P.) periods. The 198-bp ancient mtDNA was amplified from 74 dog samples, and the sequences were classified into 19 haplotypes comprising five modern haplotypes (M1, M2, M5, M10 and M11) identified in modern dogs together with ancient haplotypes showing unique sequences not observed in modern dogs. Haplotype M5 was widely distributed in archaeological sites in northern Japan and Sakhalin, while haplotype M2 was detected from sites in southern Japan. Three major clusters (CL1 to CL3) were distinguished within the modern dog control region using phylogenetic analysis; all ancient dogs belonged to the CL1 cluster.

These results suggest that the CL1 cluster was probably distributed in the Japanese archipelago from the Jomon Period. Further haplotype M2 among the CL1 was likely distributed in Japan somewhat later (around the Yayoi period).

All the data on the gene flow of dogs in Japan and east Asian regions adjacent Japan support the following hypothesis: The first dogs entered the Japanese archipelago from southern or northern continental Asia. These dogs eventually spread throughout Japan. Then other dogs were brought over via the Korean Peninsula, and crossbreeding occurred with the original dog breeds. The resulting offspring can be assumed to be the ancestors of the Japanese breeds that exist today.

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Tanabe et al.26) and Tanabe and Yamazaki27) studied breed differences using the behavioral profiles of 19–31 dog breeds including six Japanese dog breeds. Profiles were obtained from the scores judged by small animal veterinarians, veterinary nurses and dog trainers. Highly significant breed differences were observed for all traits. High scores for aggressiveness, such as territorial defense, hostility toward other dogs and dominance over owners were clearly observed in six Japanese breeds, whereas those same breeds scored low estimates in friendly scores such as demand for affection, alacrity in obedience training, and playfulness, and adaptability to new owners, in contrast to friendly breeds such as of Labrador Retriever and Golden Retriever.

Ito et al.28) surveyed the allele frequency distribution of the canine dopamine receptor D4 gene (DRD4) exon III with nucloide sequence polymorphisms in 23 breeds including a total of 1,535 individual unrelated dogs. A group of breeds in which the alleles 447b, 498 and 549 were frequent tended score higher aggression-related behavioral traits than those with frequent alleles435 and 447a. Figure 5 shows a neighbor-joining tree indicating of composition of DRD4 exon III made by the neighbor-joining method using genetic distance. Breeds were divided into two major groups, A and B. This figure shows a close relationship among four Japanese breeds, i.e. the Hokkaido, the Shiba, the Akita and the Shikoku and a Chinese breed the Shih Tzu, while breeds from the B group are more aggressive than A-group.

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Guo-Dang Wang et al., Out of southern East Asia: the natural history of domestic dogs across the world Cell Res. 2016 Jan; 26(1): 21–33. doi:  10.1038/cr.2015.147 PMCID: PMC4816135

The origin and evolution of the domestic dog remains a controversial question for the scientific community, with basic aspects such as the place and date of origin, and the number of times dogs were domesticated, open to dispute. Using whole genome sequences from a total of 58 canids (12 gray wolves, 27 primitive dogs from Asia and Africa, and a collection of 19 diverse breeds from across the world), we find that dogs from southern East Asia have significantly higher genetic diversity compared to other populations, and are the most basal group relating to gray wolves, indicating an ancient origin of domestic dogs in southern East Asia 33 000 years ago. Around 15 000 years ago, a subset of ancestral dogs started migrating to the Middle East, Africa and Europe, arriving in Europe at about 10 000 years ago. One of the out of Asia lineages also migrated back to the east, creating a series of admixed populations with the endemic Asian lineages in northern China before migrating to the New World. For the first time, our study unravels an extraordinary journey that the domestic dog has traveled on earth. …

Population genetic analysis reveals an ancient origin for the domestic dog in southern East Asia about 33 000 years ago. After evolving for several thousand years in East Asia, a subgroup of dogs radiated out of southern East Asia about 15 000 years ago to the Middle East, Africa as well as Europe. One of these out of Asia lineages then migrated back to northern China and made a series of admixtures with endemic East Asian lineages, before traveling to the Americas. Our study, for the first time, reveals the extraordinary journey that the domestic dog has traveled on this planet during the past 33 000 years.

When partitioning the individuals into two groups, the algorithm separates the dogs from the wolves, with very limited admixture observed (Figure 1D). Further dividing the individuals into three subsets split the dogs into two clusters, with indigenous dogs from southern East Asia representing one subset and the other subset consisting of dog breeds from Europe and South/Central America and the African village dogs.

Indigenous dogs from northern China and dog breeds from the Arctic and Central Asia, the Middle East and North Africa show a mixture of these components with varying proportions. This observation implies that there are two divergent groups of dogs: one is East Asian component and the other, non-East Asian component. It is important to emphasize that individuals with mixed constituents identified in the structure analysis are not always due to true admixture events, since populations of intermediate genotypes between these two groups tend to display mixed components (e.g., originated shortly after the split of two clades,Supplementary information, Data S3 and Figure S3). Further partitioning into four and five groups leads to the separation of the African village dogs and the breed dogs from the eastern Arctic regions (i.e., Siberian Husky, Alaska Malamute and the Greenland dog).

Genetic diversity among individuals (Figure 1C) may be heavily influenced by ancient as well as recent history, e.g., breeding programs during the last few thousand years or the past few hundred years. However, combined information from multiple breeds may reveal information about the ancestral populations that gave rise to them, since each breed has experienced separate breeding history. We therefore calculated the genetic diversity (θπ) for the “pure groups” informed by the structure analysis (K = 4, Figure 1D). As shown in Figure 1E, dog breeds, most of which of European origin, carry lower diversity than the Chinese indigenous dogs as a group, but have higher genetic diversity than the African indigenous dogs. This suggests that the ancestral population that gave rise to the European breeds was larger than the ancestral population of the African indigenous dogs. Linkage disequilibrium patterns also show similar trends (Figure 1F).

Principle component and phylogenetic analysis

When projecting the genotypes into a two-dimensional space using a principle component analysis (PCA)19, all dogs cluster together tightly compared with the distribution seen for wolves (Figure 1G, inset). When inspecting the distribution among dogs, we find that dogs spread along three major geographic axes: southern East Asia, Europe and Africa. The northern Chinese indigenous dogs and dog breeds from the Middle East/Arctic regions/Tibet fall between these three extremes (Figure 1G). The observed pattern reflects the overall geographic locations of these groups following a clear East-West gradient, which matches quite well the observation from our structure analysis.

Combining our dataset with data from a previous SNP array study, which included a larger number of samples20, we found that the southern Chinese indigenous dogs together with several East Asian dogs (e.g., Chow Chow, Akita, Chinese Shar-Pei) are closest to wolves (Figure 1H). When the phylogenetic relationships among our 58 samples are inspected, East Asian dogs spread over both sides of the deepest node connecting all dogs, while dogs from other continental areas coalesce into a subclade and then join with East Asian dogs. Thus, East Asian dogs are the most basal lineages connecting to gray wolves (Figure 1I). It is worth pointing out that the genomes of dogs from Oceania (dingoes and New Guinea singing dogs), although being closer to wolves in the PCA plot (Figure 1H), bear strong signals of admixture with gray wolves6, which likely reflects their past history of admixture, before they migrated to Australia and New Guinea (Supplementary information, Data S4 and Figure S4).

Admixture analysis

Using the joint allele frequencies among all populations in our study, we infer the split and admixture history among groups of populations using TreeMix21. If migration tracks are not allowed, then the relationships inferred from the TreeMix analysis (Figure 2A) directly reflect the patterns observed in our previous analyses including the structure (Figure 1D), the phylogenetic (Figure 1I) and the principal component analyses (Figure 1G). Thus, following the divergence between contemporary wolves and domestic dogs, the first partition within dogs is between the southern Chinese indigenous group and all other dogs. This is then followed by branching of the other dogs, largely matching the geographical distance from southern East Asia: first, dogs from Central Asia, northern China, and eastern Arctic, followed by dogs in Africa, the Middle East, and western Arctic, and the final group including all dog breeds in Europe and South/Central America.

Figure 2

Demographic and migration histories for the domestic dog. (A) Tree topology inferred from TreeMix when no migratory tracts are allowed. The drift parameter is the amount of genetic drift along each population. Further inferred migratory tracts are shown

If migration tracks are allowed in TreeMix, there is strong statistical support for migrations among a few groups: (1) northern Chinese indigenous dogs show strong admixture from European dogs (Figure 2A and Supplementary information, Data S5, Figure S5, Tables S2 and S3); (2) gene flow from wolves to the African/Middle Eastern dogs (Supplementary information, Figure S5); (3) migratory tracks from the southern Chinese dogs to the eastern Arctic group (i.e., Siberian Husky, Alaska Malamute and the Greenland dog; Supplementary information, Figure S5). When all possible migration events in the history of these samples are examined using the F3/F4 test22, there is again a strong statistical support for all the migration events listed above (Supplementary information, Data S5).

Long-term evolutionary trajectories for wolves and dogs

Using the divergence between the two haploid genomes within individuals, the pairwise sequentially Markovian coalescent (PSMC) model provides a method for investigating the long-term trajectories in population sizes23. To translate demographic history into real-time units, estimation of an accurate mutation rate is very important. Previously, several different mutation rates were used, but they were generally not carefully calibrated (Supplementary information, Data S6)24. Using multiple outgroup species to the dog (e.g., horse and cat), our estimate of the mutation rate for the lineage leading to the domestic dog is 2.2 × 10−9 per site per year (Supplementary information, Data S6 and Table S4), a rate similar to those from several earlier studies25,26. Using this mutation rate, we estimate dates for the population history of dogs and wolves. As shown in Figure 2B, a decrease in the size of the ancestral wolf population started to occur 2 million years ago, reaching a saddle point about 3-400 000 years ago. The ancestral population then increased in size, peaking at around 200 000 years ago. After a subsequent small decline in population size, wolves and dogs started to diverge from each other between 20 000 and 100 000 years ago (see next section for a more precise dating). Although all domestic dogs drastically decreased in population size after the population split, the wolf population experienced a slight growth, possibly as a consequence of the megafauna extinctions (i.e., late Quaternary extinction)27 that provided gray wolves with better food resources due to reduced competition from other predators.

Time of divergence between contemporary wolves and dogs

Treemix and phylogenetic analyses identified southern Chinese indigenous dogs as the most basal population compared to wolves, from which all other dog populations diverged. We therefore used joint allele frequencies between the 12 gray wolves and the 11 southern Chinese indigenous dogs, to infer the demographic history for these two populations with the dadi package28. Similar to the result from the PSMC analysis, the wolf population experienced a very mild population growth (1.26-fold increase) that started around 290 000 years ago (Figure 2C). The time of divergence for the wolf and dog populations is inferred to be around 33 000 years ago, where the domestic dog lineage expanded from a population of 4 600 individuals to about 17 500.

In addition to gauging changes in population size, statistical methods can also estimate the rates of exchange of migrants between two populations. The migration rate (2Nm) from the dog lineage to the wolf lineage is estimated to be 0.97, while the other direction (wolves to dogs) is inferred to be 5.02, showing a clear asymmetry in the migration rates29.

Examination of the sequence divergences between the multiple populations using a Markov chain Monte Carlo (MCMC) approach30,31 (Supplementary information, Data S7, Figures S6-S8, Tables S5 and S6) reveals a similar profile for the history between wolves and dogs, which includes a slight growth in the wolf population and an ancient divergence between wolves and dogs (Supplementary information, Data S7 and Table S5). In summary, multiple levels of genetic information (i.e., both joint site frequencies as well as sequence divergence) support an ancient split between dogs and wolves.

The geographical origins of dogs: a single origin in southern East Asia

In order to identify the most probable geographical origin of dogs, we hypothesized that similar to many organisms, the geographical origin of a species holds the greatest genetic diversity, and the global relationship among multiple populations will, in the absence of strong influence of admixture, follow a serial founder model32,33. In the case of dogs, the wild ancestor, the wolf, has been present along the dog throughout Eurasia, implying that intense dog-wolf admixture could possibly have influenced this pattern.

Despite the concern on the confounding effect of wolf/dog gene flow, the TreeMix analysis, F3/F4 test as well as the demographic analysis suggest that gene flow between dogs and wolves is relatively mild. In Supplementary information, Data S8, we review the evidence for dog/wolf gene flow from our study, as well as from multiple previous studies. The combined evidence shows that the migration rates (2Nm) are mostly around one or less (a maximum of five found in the dadi analysis) and that the admixture proportion is normally around 10%, with a maximum of 16% for the Middle East (Supplementary information, Data S8). Low levels of migration are detected between wolves and dogs across Eurasia when the very sensitive D test is used34,35 (Supplementary information, Data S8). Thus, we conclude that while dog-wolf gene flow has occurred throughout history of the domestic dog, it has been at a moderate level and the level of admixture has been relatively similar across Eurasia (Supplementary information, Data S8). Without the strong influence of admixture32, we may assume that genetic diversity is highest at the place of origin and that the global relationship among the multiple populations follows a serial founder model reflecting their dispersal routes33.

It is tempting to draw conclusions about the origin of dogs from the high genetic diversity observed in the Chinese indigenous dogs. However, comparing breed dogs with indigenous dogs at the individual level is likely misleading since most of the differences in genetic diversity are probably caused by recent bottleneck events rather than their distant origin1. Thus, we combine multiple breeds in each region as a group representing the ancestral haplotype pool giving rise to the contemporary dogs of that region. Our analysis shows that dogs from East Asia have the highest genetic diversity (Figure 1E). This suggests that the ancestral population that gave rise to East Asian dogs was much larger than ancestral populations in other regions (e.g., Europe). The linkage disequilibrium pattern also shows the same trend (Figure 1F). Higher levels of genetic diversity in East Asian dogs are also observed in mtDNA and Y chromosome data7,12,36.

Beside group diversity, in the phylogenetic and TreeMix analyses, the deepest node connecting all dogs separates into two clades, one of which is composed of only East Asian dogs, while the other clade includes both East Asian and non-East Asian dogs (Figures 1I and and2A,2A, and Supplementary information, Figure S5). Dogs from Africa and Europe share a most recent common ancestor, which then coalesces with dogs from East Asia (Figures 1I and and2A).2A). Notably, this basal position of East Asia is robust to the levels of migrations between wolves and dogs (Supplementary information, Data S9, Figure S9, and Table S7). The basal position of East Asian dogs is similar to the pattern observed for Africans within human populations37.

In addition to the observations based on group level diversity and the basal phylogenetic position, the PCA pattern also provides supporting evidence for the southern East Asian origin of dogs. As the amount of genetic drift in basal groups is typically lower due to their larger population sizes, we expect them to display a closer genetic relationship with wolves in the PCA plot (Figure 2A). When we simulate a serial founder model that mimics the history of dog domestication, we can easily generate a pattern that is similar to that shown in Figure 1G (see also Supplementary information, Data S10 andFigure S10). Thus, in our analysis, we find dogs with ancestry in southern East Asia to be closest to wolves, and also a geographical distribution of the populations following a clear east-west gradient, indicating serial founder events. It is important to emphasize that admixture between wolves and dogs is unlikely to have created the observed pattern, given that the dog-wolf admixture rate in East Asia is not higher than that seen in other regions (Supplementary information, Data S8).

Having identified southern East Asia as the likely origin of dogs, we asked whether the domestic dog may have originated in more than one region through separate domestication events. In order to test whether multiple origins are compatible with the observed data, we performed simulations mimicking different scenarios (Supplementary information, Data S11 andFigure S11). Our results show that, if there were multiple origins for dogs from separate wolf populations, the descendant populations would tend to reside in separate clusters in the PCA plot, which is in contrast to what we observe (Figure 1G, inset). Thus, that the domestic dog originated multiple times in different geographical areas is not compatible with the observed genetic patterns found in our genome data.

The out of southern East Asia history for the domestic dog

To study the subsequent global history of the dog, we used an MCMC approach to date several important transitional points among the major clades (Figure 2A). Our analysis supports the split between the southern Chinese indigenous dogs and all other dogs across the world around 15 000 years ago, thus indicating a radiation of dogs out of southern East Asia earlier than the origin of agriculture (Supplementary information, Data S7 and node 2 in Figure 2A and and2D2D)38. After radiating from southern East Asia, possibly following existing human settlements at the time (Supplementary information, Data S12 and Figure S12), the out of southern East Asia lineage spread to the Middle East/Africa and arrived in Europe by about 10 000 years ago (Supplementary information, Data S7; node 3 in Figure 2A and and2D).2D). Notably, one of the out of southern East Asia lineages migrated back to northern China, meeting endemic Asian lineages that had spread from southern East Asia and yielding a series of admixed populations, including the northern Chinese indigenous dogs and the Arctic dog breeds (Figure 2Aand and2D2D).

Several dog breeds from South and Central America (i.e., Chihuahua, the Mexican and Peruvian naked dog) show no signs of admixture, while the Arctic breeds, Alaska Malamute and the Greenland dog, display extensive admixture from the southern Chinese Indigenous lineage39. Possibly, this reflects that the human colonization of the New World occurred in several waves, in which dogs may have followed in different time periods40 (Figure 2D). Using the patterns of the admixture tracks, we estimate that the time of the admixture for the northern Chinese indigenous dogs was quite ancient (around 10 500 years ago, Supplementary information, Data S13 andFigure S13)40. The relatively recent origin of European dogs (i.e., ∼10 000 years) together with this rather ancient admixture suggests that multiple lineages travelled to the Far East from the Middle East/Europe.

Population structure among wolves

Our structure and principal component analyses do not reveal any population substructure among the gray wolves collected for this study (Figure 1D). The high migratory ability of the gray wolf might allow the populations to remain highly homogenous across the eastern part of Eurasia41. A previous study using wolves from the Middle East (Israel), Europe (Croatia) as well as China found genetic differentiation among these wolf populations6. When these three individuals are overlaid on the large PCA plot, the wolves from western Eurasia do not group together with the wolves we collected from eastern Eurasia, and they are genetically closer to dogs (Supplementary information, Data S14 and Figure S14). Given the fact that Middle Eastern wolves generally have more dog admixture6, the observed difference might not represent true population differentiation among wolves. Nevertheless, it is possible that some wolves have recently diverged from each other8, as there is weak isolation between the wolves from eastern and western Eurasia. Explicit testing for potential admixture between wolves and dogs sampled in our study finds evidence of gene flow between wolves and local dog populations in each region, albeit the magnitude is low (Supplementary information, Table S8). Further study on the genetic and geographic relationships between dogs and wolves is one of the important tasks for the community.

Domestication genes

Our analyses indicate that the Chinese indigenous dogs represent an intermediate form between wolves and breed dogs, and they have not experienced intense artificial selection. Analyses of Chinese indigenous dogs therefore allow us to stratify the domestication process in dogs, and investigate the role of positive selection that occurred specifically during the first stage of domestication. Using a statistical method that explicitly models selective sweeps42, we have identified the top 1% of the genome bearing strong statistical evidence of positive selection in the southern Chinese indigenous dogs. In Table 1, we list the categories of genes that show statistical significance by a gene enrichment-based analysis. Groups of genes showing the strongest evidence of positive selection are those related to metabolism and motility, neurological process and perception as well as sexual reproduction (Table 1 and Supplementary information, Data S15,Tables S9 and S10). Genes that seem to have been positively selected in subsequent evolutionary steps, including dog breed formation, are related to the control of developmental processes and to metabolism (see a full discussion of candidate genes involved in transforming wild wolves to dogs in Supplementary information, Data S15).

Table 1

Gene ontology analysis of genes selected during the first stage of dog domestication

Among the candidates as positively selected genes in the first stage of dog domestication, a class of genes are related to memory and long-term potentiation (LTP), which is widely considered to be the major cellular mechanism underling learning and memory43. For example, GRIA1 (glutamate receptor, ionotropic, AMPA 1) is an important protein that mediates excitatory synaptic transmission in the central nervous system and plays a key role in hippocampal synaptic LTP and long-term depression (LTD). Interestingly, a suite of other genes, including GRIN2A (glutamate receptor, ionotropic, N-methyl D-aspartate 2A), are also found to be heavily involved in LTP and LTD (Table 1). The large physiological and behavioral changes empowered by these genes may have enabled the transformation of gray wolves to domestic dogs, allowing them to flourish in the human environment.

Discussion

Based on genome sequences from a worldwide collection of dogs, especially a large collection of indigenous dogs from southern East Asia, this study provides strong genetic evidence that the domestic dog originated in southern East Asia. The analyses give a coherent picture, where the indigenous dogs in southern East Asia or East Asia in general stand out compared to other populations, with higher genetic diversity as a group, and occupying a basal position next to wolves. Other dog populations show progressive ancestry gradient away from wolves starting from southern East Asia. Notably, these findings corroborate earlier work based on mtDNA and Y-chromosomal DNA7,36. Thus, studies based on comprehensive global samples and diverse types of genetic data (e.g., autosomes, Y chromosome, mtDNA) converge on the same story about the origin of the domestic dog.

The origins of the global domestic dog populations can be traced to two important demographic steps: first, dog and wolf populations started to diverge from each other 33 000 years ago in southern East Asia (matching several previous findings8,10). Subsequently there was a global dispersal of dogs out of southern East Asia around 15 000 years ago. The long persistence of the domestic dog lineage in southern East Asia opens up for interesting scenarios. One possible explanation for the 33 000-year deep divergence between dogs and wolves is that it represents a split among wolf populations, and that South Chinese wolves (ancestors to the dog) were genetically differentiated from the more northern wolves sampled in our study. In this case, the global expansion of dogs out of southern East Asia around 15 000 years ago may correspond with the origins of actual domestic dogs. This scenario is contradicted by the fact that wolves in our study display no apparent genetic substructure (Supplementary information, Data S14). An alternative scenario is that the ancient dog-wolf split actually constitutes the first step in the domestication of wolves and evolution to domestic dogs. It is possible that the ecological niche unique in southern East Asia provided an optimal refuge for both humans and the ancestors of dogs during the last glacial period (110-12k years ago, with a peak between 26 500 and 19 000 years ago)44. The mild population bottleneck in dogs suggests that dog domestication may have been a long process that started from a group of wolves that became loosely associated and scavenged with humans, before experiencing waves of selection for phenotypes that gradually favored stronger bonding with humans (a process called self-domestication)1. That among the candidate genes as positively selected are genes involved in the neurological processes may be a manifestation of this dynamic process (Supplementary information, Data S15). After this long-term nurturing, humans and dogs might have eventually come together with a strong bond for each other. Thus, the history of dogs might involve three major stages: (a) loosely engaged pre-domesticated scavengers, (b) domesticated non-breed dogs with close human-dog interactions, (c) breed formation following intense human selection for diverse sets of phenotypic traits. The study of Chinese indigenous dogs thus provide missing links that connect these three major stages45,46.

The exact time when dogs reached the Middle East is difficult to estimate with our sample since the Middle Eastern dogs (and also African dogs) bear relatively strong signals of introgression from wolves (Figure 2A). However, demographic inferences suggest that dogs had arrived in Europe by about 10 000 years ago (Figure 2D and Supplementary information, Data S7), a short time after the origin of agriculture in the Middle East38. It is notable that the global spread of dogs around 15 000 years ago corresponds well with the generally accepted earliest archaeological evidence of dogs across Eurasia11. As there is little evidence of westward human migrations from southern East Asia around 15 000 years ago, the initial spread of the domestic dog out of Asia may in part have been a self-initiated dispersal driven by environmental factors (e.g., the retreat of the glacial coverage that started about 19 000 years ago). The specific route domestic dogs used to migrate to the Middle East, Africa and Europe remains to be uncovered (Figure 2D and Supplementary information, Data S12). Some of this dispersal might be heavily influenced by humans, as dogs were often part of the civilization package that traveled together as agriculture spread47 (Figure 2D). Further studies using samples from western Eurasia should reveal insights into these early dog migrations6.

Despite the strong patterns presented by the genetic data, archaeological evidence supporting an East Asian origin is missing11. Several important factors further confound current analysis. First, the morphological differences between dogs and gray wolves are not always very clear-cut, especially for specimens from the early phase of dog domestication48. In fact, a recent ancient DNA study has ruled out several ancient dog-like specimens found in Europe13. Second, archaeological studies in the Far East are generally lagging behind those in Europe, with most of the ancient dog-like fossils from before 12 000 years ago being found outside of East Asia11. This could also be due to the unfavorable environmental conditions for preserving fossils in southern East Asia. Nevertheless, it is possible that multiple primitive forms of the dog existed, including in Europe13,49. However, in this case, the genetic pattern presented here shows that those lineages were replaced by dogs that migrated from southern East Asia, and thus made negligible contributions to the modern dog gene pool (Figure 1D).

This study opens many potential avenues for future research (Figure 2D). For example, the history of the American colonization and the scale of wolf-dog admixture in the Middle East and Africa remain largely unexplored, especially given the limited coverage of our African samples50. Analysis of additional samples from other parts of the world (especially the Indian coastal region and northern Eurasia as well as Africa) should allow us to draw a more complete picture of the worldwide migration patterns, and their association with human populations. Comprehensive analyses of ancient canid genomes will provide genetic information from multiple time points for elucidating the initial steps of dog history, and identifying putative population replacements that may have influenced modern day dog’s gene pool8.

The study of Chinese indigenous dogs has provided an unprecedented opportunity for illuminating the history of selection during dog domestication. For example, the initial selection on the domestic dog is found be strongly associated with an enrichment of genes affecting behavior and motility. As dogs established stronger bonds with humans, possibly empowered by the origin of modern agriculture in the Middle East and China51, strong selection for genes involved in metabolism and morphology/development emerged (Supplementary information, Data S15). Our study, for the first time, begins to reveal a large and complex landscape upon which a cascade of positive selective sweeps occurred during the domestication of dogs. The domestic dog represents one of the most beautiful genetic sculptures shaped by nature and man

Brown SK, Phylogenetic distinctiveness of Middle Eastern and Southeast Asian village dog Y chromosomes illuminates dog origins. PLoS One. 2011;6(12):e28496. doi: 10.1371/journal.pone.0028496. Epub 2011 Dec 14.

Archaeology and DNA studies indicate that dogs evolved from or share a recent common ancestor with the gray wolf (Canis lupus) 12,000–40,000 years BP, and that they spread rapidly throughout Eurasia and the Americas at the end of the last ice age [1][6]. However, controversy persists over where dogs originated, with most evidence cited in favor of Europe [7][9], the Middle East [10][12], or Southeast Asia [6], [13], [14]. One problem potentially confounding this question is uncertainty in the links between extant dogs and the original canine inhabitants of those same regions.

This study, after a larger sampling from dogs in the south of East Asia, found the highest genetic diversity from Southeast Asian dogs.

“Numbers of accumulated mutations between ancestral and descendent nodes (i.e., ρ estimates) also were consistent with an older Southeast Asian than Middle Eastern Y chromosome clade, possibly a reflection of effective population size more so than population age, but, nevertheless, of higher diversity in the Southeast. Thus, it seems well-supported based on both matrilineal and patrilineal markers that extant dogs of Southeast Asia, over an even larger region than that identified by Pang et al. [14] and including near Island Southeast Asia, harbor more genetic diversity than the Middle East. Although these findings do not constitute proof that dogs originated in Southeast Asia[12], [20], [45], they clearly indicate continuity with a very ancient dog population in that region and, therefore, that it likely played an important role in the evolution of modern dogs.”

The study further found that “the European and American breeds clustered almost entirely within the Southeast Asian clade, even sharing many haplotypes, suggesting a substantial and recent influence of East Asian dogs in the creation of European breeds. Comparison to 818 published breed dog Y STR haplotypes confirmed this conclusion and indicated that some African breeds reflect another distinct patrilineal origin. The lower-resolution mtDNA marker consistently supported Y-chromosome results. Both marker types confirmed previous findings of higher genetic diversity in dogs from Southeast Asia than the Middle East.”

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The results of the above study were further confirmed by another 2012 study.

Ding ZL et al., Origins of domestic dog in southern East Asia is supported by analysis of Y-chromosome DNAHeredity (Edinb). 2012 May;108(5):507-14. doi: 10.1038/hdy.2011.114. Epub 2011 Nov 23.

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Abstract

Global mitochondrial DNA (mtDNA) data indicates that the dog originates from domestication of wolf in Asia South of Yangtze River (ASY), with minor genetic contributions from dog-wolf hybridisation elsewhere. Archaeological data and autosomal single nucleotide polymorphism data have instead suggested that dogs originate from Europe and/or South West Asia but, because these datasets lack data from ASY, evidence pointing to ASY may have been overlooked….Two haplogroups were universally shared and included three haplotypes carried by 46% of all dogs, but two other haplogroups were primarily restricted to East Asia. Highest genetic diversity and virtually complete phylogenetic coverage was found within ASY. The 151 dogs were estimated to originate from 13-24 wolf founders, but there was no indication of post-domestication dog-wolf hybridisations. Thus, Y-chromosome and mtDNA data give strikingly similar pictures of dog phylogeography, most importantly that roughly 50% of the gene pools are shared universally but only ASY has nearly the full range of genetic diversity, such that the gene pools in all other regions may derive from ASY. This corroborates that ASY was the principal, and possibly sole region of wolf domestication, that a large number of wolves were domesticated, and that subsequent dog-wolf hybridisation contributed modestly to the dog gene pool.

our data indicate that the Y-chromosome genepool of the relatively limited number of dog samples in this study originates from at least 13–24 different wolf Y-chromosome haplotypes. The formation of the dog haplotypes in five star-like clusters must therefore partly stem from the relations between haplotypes in the founder wolf population(s). Notably, an origin of dogs from numerous male wolves is in line with both mtDNA data indicating that dogs originated from a minimum of 51 female wolf lineages (Pang et al., 2009) and MHC data (from the low diversity European dog population) indicating an origin from at least 21 wolves (Vilà et al., 2005). Therefore, multiple genetic datasets indicate that dogs originate from a large number of domesticated wolves.

Two of four principal haplogroups are shared universally but two are almost exclusive to East Asia

The dog Y-chromosome gene pool was to a large degree shared among the populations across the world (Figures 1b and c). Two of the five haplogroups (HG1 and HG23) were virtually universally represented and carried by 62% of all dogs in the study. The three central haplotypes within these haplogroups, H1, H1* and H23*, were carried by almost half (46%) of the dogs and shared by dogs in Europe, SW Asia and China, by 75%, 44% and 32% of the individuals, respectively.

However, there were also distinct differences in the geographical representation and distribution of haplogroups and haplotypes. The other three haplogroups were also distributed across relatively large distances but not universally spread. HG3 was found in East Asia (including Siberia) and America, and at lower frequency in SW Asia, Scandinavia and Britain, but not in samples from the European continent and Africa. HG6 was found in East Asia and at low frequency in SW Asia, but was absent elsewhere. Finally, HG9 was found in only totally four individuals, but as far apart as East Siberia (one individual) and Central Africa (three individuals).

As the sample sizes were relatively limited, haplogroups with low frequency, for example, HG9 may have remained undetected in some populations. However, the general pattern was that the four main haplogroups were relatively equally represented in the eastern part of the world, whereas west of the Himalayas and the Urals haplogroups HG1 and HG23 were represented by 89% of the individuals, and HG6 and HG3 rare or absent. Thus, HG1 and HG23 were universally represented, whereas HG3 and HG6 had restricted distributions. Only in East Asia and SW Asia all four major haplogroups were represented.

Highest genetic diversity in Southwestern ASY

Accordingly, except for the practically universal representation of haplotypes H1, H1* and H23*, the representation and frequencies of haplotypes differed considerably among regions, as demonstrated in the phylogenetic trees (Figure 1c). In some regions, for example, Europe, frequency was very high for a few haplotypes, mainly H1, H1* and H23*, and other parts of the phylogeny was empty. Other regions, for example, ASY, had a larger number of haplotypes at more even frequencies and representation across the phylogeny. These differences in genetic coverage are reflected in difference in genetic diversity measured as the number of haplotypes per sampled individual and HD (Table 1). In many cases the samples were too small to yield significant differences, but the general trend was that the highest values for genetic diversity among all regions were found within ASY, there were medium values in other parts of East Asia, and in SW Asia and Africa, and low in Europe and America.

Comparing the three major regions suggested as potential origins for dogs, ASY had the highest diversity with 13 haplotypes among 23 samples, and a HD of 0.901, to compare with SW Asia and Europe, which had 9.58 and 6.50 haplotypes at resampling of 23 samples, and a HD of 0.863 and 0.734, respectively (Table 1). Importantly, except for haplogroup HG9, practically the full diversity for dog Y-chromosome DNA was covered in ASY, such that all haplotypes in other regions were maximally one step from haplotypes in ASY (Figure 1c). The highest diversity worldwide was found within the Southwestern part of ASY (Southw ASY; Southeast Asia and the adjacent Chinese provinces Yunnan and Guangxi) with 11 haplotypes among 16 individuals, 10.10 haplotypes at resampling size 14, and a HD of 0.950. In contrast, at the other end of Eurasia, Europe had 7 haplotypes among 32 samples and 5.31 haplotypes at resampling size 14, almost half compared with Southw ASY. The remarkably low diversity for Europe is related to high frequency of haplotypes H1 (carried by 47% of the individuals) and H1*(22%) and that the other parts of the phylogeny are largely empty. This pattern was shared across Europe, by the north and south parts of the continent as well as Britain, and must therefore stem from the first origin of the European-dog population and not from later intense breeding, as it is unlikely that all haplogroups but HG1 would have been lost independently in several different lineages leading to today’s breeds. SW Asia had 10 haplotypes among 25 samples and 7.35 haplotypes at resampling size 14, and had much higher frequency of haplogroup HG23 (68%) than other regions, whereas only one and two samples carried HG3 and HG6, respectively. Within SW Asia, the Fertile Crescent region (Fertile Cr; West Iran, Israel and East Turkey) had a higher diversity, with HD higher, but the number of haplotypes lower than ASY. Also here the frequency of HG23 was high (57%), but all four main haplogroups were represented. Among other regions, Siberia had especially high diversity, with marginally lower values than Southw ASY for number of haplotypes and haplotype diversity. Central and N China and Africa had medium diversity values and the small sample of American dogs had three haplotypes among nine samples.

Thus, diversity differences were generally small across the Old World, but Southw ASY had the highest diversity of all regions. The large difference between the opposite sides of the Eurasian continent is striking, and further highlighted by comparing the samples from Europe, having seven haplotypes among 32 samples, and Southeast Asia with six haplotypes (distributed among all four major haplogroups) among only 7 samples (Figure 1c).

With this study, two independently inherited markers have shown genetic diversity among dogs worldwide to be highest within ASY. It is also notable that, in similarity to the mtDNA data, ASY had the most comprehensive coverage of the phylogenetic diversity of all regions. The haplotypes were distributed across the four major haplogroups such that all haplotypes in other regions were at most one substitution from a haplotype found in ASY (Figure 1c). Therefore, except HG9, all haplotypes across the world were identical to or differed by a single substitution from a haplotype found in ASY, and may potentially have derived from haplotypes present in ASY.

A possible single origin of all haplogroups in ASY, but not in SW Asia or Europe

The haplogroups were geographically distributed in a distinct pattern (Figure 1b). HG1 had a frequency close to 100% in Europe and Africa, and HG23 a high frequency in SW Asia and Central China, but both haplogroups were also represented at lower and relatively even frequency virtually worldwide. In contrast, HG3 and HG6 were almost exclusively restricted to East Asia, at moderate frequency. This pattern may be explained by an origin of all four haplogroups from a single (not necessarily homogenous) founder population somewhere in East Asia, for example ASY, and genetic bottlenecks reducing diversity in other populations. However, separate origins of the haplogroups in different regions followed by non-symmetrical migrations between populations are also possible.

The high frequency (81%) and large number of haplotypes (four) of HG1 in Europe could possibly be explained by an origin of HG1 in Europe, after which only two of four haplotypes derived from the wolf founders would have spread to other regions. However, because of the high frequency in Europe of this haplogroup, a larger number of derived haplotypes are expected than in other regions. Among the 26 European lineages carrying HG1, 0.60–2.51 substitutions (0.57–2.60, 95% confidence limits) would be expected to have occurred during the 11 500–16 000 years since the origins of dogs. This indicates that only the universal haplotypes, H1 and H1* were inherited from wolf and the others derived from mutations within the European dog population. Therefore, HG1 being virtually universally represented, its geographical origins cannot be definitely identified based on this dataset. Similarly, SW Asia had a high frequency (68%) and the largest number of haplotypes (five) of HG23. In this case, 0.39–1.64 (0.37–1.70) substitutions would be expected among the 17 lineages in SW Asia, weakly indicating that HG23 may have originated in SW Asia. It is notable that the Fertile Cr had four haplotypes among eight individuals carrying HG23. However, HG23 was represented almost universally and also ASY had a high diversity for HG23, with three haplotypes among three samples. For HG3, ASY had six haplotypes among eight lineages. Only 0.18–0.77 (0.18–0.80) substitutions would be expected since the origins of dogs, leaving the majority of haplotypes identical to the haplotypes carried by wolves; the star-like formation of HG3 was obviously inherited from the founder wolf population. The large number of HG3 haplotypes in ASY indicates an origin of this haplogroup in ASY or adjacent regions, but a relatively high diversity (four haplotypes among six individuals) in Siberia is also notable. Finally, HG6 being found almost exclusively in East Asia most probably originated somewhere in this region.

Consequently, it is not possible to definitely point out from where each haplogroup originated. However, it can with greater certainty be concluded from where the haplogroups did not originate. Thus, it seems very unlikely that haplogroups HG3, HG6 and HG23 would have originated in Europe or Africa, or haplogroups HG3 and HG6 in SW Asia. Therefore, three out of four of the dogs Y-chromosome genepool clearly originates from outside Europe as only HG1 may have originated there. Importantly, the extremely low diversity in Europe cannot be linked to the intense breeding of European dogs in historic times (see Discussion). It also seems clear that a maximum of roughly 50% of the genepool (HG23 and HG1) may have originated in SW Asia. In contrast, the full dog Y-chromosome gene pool may have originated somewhere in East Asia, including ASY. ASY is especially likely considering that, uniquely, all haplotypes of the four major haplogroups differed by at most one substitution from haplotypes in ASY.

To conclude, the Y-chromosomal DNA data indicates that if the domestic dog originated from a single geographical region this could have happened in ASY but not in SW Asia or Europe. If the dog originated from several regions, at most 50% of the gene pool may have originated in SW Asia or Europe. Thus the Y-chromosome data indicates that wolves in ASY were the major source of genetic diversity for dogs.

Discussion

With this study, analyses of two independently inherited DNA markers, the only two studies based on global samples of dogs performed so far, give strikingly similar pictures of dog phylogeography. Thus, both the present study of Y-chromosomal DNA and earlier studies of mtDNA (Pang et al., 2009) show that ∼50% of dog genetic diversity is shared in a universal gene pool, but whereas most regions harbour only these 50%, ASY has virtually the full range of genetic diversity from which the complete gene pools in other regions may derive. It is unlikely that the two datasets would by chance have obtained the same phylogeographical pattern or that selection would have affected both markers similarly. Therefore, these results offer strong evidence that domestication of wolf occurred primarily and possibly exclusively in ASY, with only small genetic contributions from wolf in other regions, through dog–wolf hybridisation.

This is in conflict with conclusions normally drawn from analyses of the archaeological record (Clutton-Brock, 1995) and in a recent study of autosomal SNPs (Vonholdt et al., 2010), suggesting SW Asia and/or Europe as the principal regions of origin. However, both the archaeological record and the SNP study suffer from geographical bias in a lack of data from ASY (Klütsch and Savolainen, 2011). Therefore, there is a clear possibility that these datasets failing to identify ASY’s central role in dog origins may reflect the lack of sampling specifically from this region. Arguably, the Y-chromosome DNA and mtDNA datasets represent only two genetic markers, and the Y-chromosome data includes relatively small samples. Therefore, analyses of further markers are desirable; when based on comprehensive sampling, large-scale studies of genome wide polymorphisms, for example, autosomal SNPs will help to reveal dog history in unprecedented detail. However, in the light of the mtDNA and Y-chromosomal data, comprehensive sampling from ASY is necessary for any study aimed at unravelling the origins and earliest history of dogs. It is especially notable that, for both Y-chromosome and mtDNA data, diversity is much lower in N China and Central China than in ASY, and instead more similar to that of other regions, for example, SW Asia. Therefore, samples from China or East Asia in general cannot compensate for lack of samples from ASY.

The exact geographical origin of each Y-chromosome haplogroup cannot be determined based on the present dataset. However, it seems clear that at most 50% of the genetic diversity can have originated from SW Asia or from Europe, and it is possible, especially considering that all haplotypes of the four principal haplogroups differ by at most a single substitution from a haplotype found in ASY, that 100% of the Y-chromosome gene pool originated in ASY in a single domestication event. The strongest indication against this is the high frequency and relatively high diversity of HG23 in SW Asia. In Fertile Cr >50% of the samples had HG23 and four of the six haplotypes were represented, suggesting the possibility of a separate origin of HG23, through independent domestication or crossbreeding of dog and wolf. However, in the case of independent domestication a high frequency would be anticipated also in the neighbouring regions, but instead the frequency of HG23 was exceptionally low in, for example, Europe (6%). Considering the large impact of the spread of farming and the related farm animals from the SW Asia to Europe (Bellwood, 2005), it would be anticipated that European dogs, if originating from SW Asia, would have a high frequency of the SW Asian haplotypes. An alternative possibility is that HG23 originated from crossbreeding of dog with wolf in SW Asia. The mtDNA data gives a clear indication of crossbreeding in SW Asia, haplogroup d2 being found only in SW Asia and the Mediterranean at a frequency of ∼2% (Pang et al., 2009;Klütsch et al., 2010). However, in crossbreeding of wolf into an already established dog population the novel haplotypes would be expected to remain at low frequency, like the mtDNA haplogroup d2, and not above 50% as HG23. The geographical origin of HG23 is therefore unclear, but an origin in ASY, where three different HG23 haplotypes were found among only three dogs, cannot be excluded.

There was not a single example of regionally restricted Y-chromosome haplogroups and therefore no clear sign that crossbreeding between male wolf and female domestic dog have contributed extensively to the evolution of the domestic dog. However, haplotypes deriving from crossbreeding would normally have limited geographical spread unless a superior phenotype would have evolved (Pang et al., 2009; Klütsch et al., 2010), and may have gone undetected in this study. So far, the only clear genetic evidence of wolf–dog crossbreeding is the regionally restricted mtDNA haplogroups d1 (restricted to Scandinavia), d2 (restricted to the Middle East and the Mediterranean), and F (found only in a few extant Japanese dogs and samples from extinct Japanese wolf) (Ishiguro et al., 2009; Pang et al., 2009; Klütschet al., 2010).

Care was taken to obtain extensive and representative samples from each geographical region, by collecting across the regions and normally a single sample from each location. It is therefore noticeable that several extensive regions had one haplotype at very high frequency (See Supplementary Dataset 3), a pattern not seen for mtDNA (Pang et al., 2009). For example, 6 of 10 samples from across Iran carried haplotype H23*, all 4 samples from (different parts of) the Japanese main island Honshu, carried H5 and 2 out of 2 samples from each of the South Chinese provinces Guizhou and Hunan carried H6. At analysis of Y-chromosome microsatellites according to (Bannasch et al., 2005) all samples had different haplotypes (SeeSupplementary Text), showing that the sharing of SNP-based haplotypes is not the result of events in modern time. Therefore, the dominance of a single Y-chromosome haplotype across large regions possibly reflects involvement of relatively few males in some migrations and population founder events.

Considering the intense breeding of European dogs during the last few 100 years, giving severe breed-specific bottlenecks (Clutton-Brock, 1995), special care was taken to avoid sampling bias by sampling a single individual per breed, from different morphological types and from across Europe. The extremely low diversity, 81% of European dogs carrying HG1, must therefore stem from before breeding started, as it is unlikely that all haplogroups but HG1 would have been lost independently in several different lineages leading to today’s breeds. For mtDNA the picture is even clearer, with the European population lacking 6 of the 10 principal haplogroups, 5 of which are missing also in SW Asia (Pang et al., 2009), showing that the loss of diversity occurred before the European and SW Asian populations were originally formed. Therefore, the low genetic diversity of the European population, and its separate grouping in analysis of autosomal SNPs (Vonholdt et al., 2010), seem to reflect the geographical position at the far end of the Eurasian continent compared with ASY, rather than recent intense breeding.

The Y-chromosome data, as well as mtDNA (Pang et al., 2009) and autosomal MHC data (Vilà et al., 2005), indicates that a large number of wolves were founders for the domestic dog population. Considering the relatively small sample of dogs in this study and that some domesticated wolves probably carried identical HTs, a minimum of 13 Y-chromosome haplotypes and 51 mtDNA haplotypes (Pang et al., 2009) deriving from the wolf founders indicates that the origin of dogs involved taming of several hundred wolves and was a major event in the related human culture.

The phylogeographical data is not detailed enough to indicate exactly where this domestication may have taken place, since several South Chinese provinces and also, for example, Burma have not been analysed for either Y-chromosome DNA or mtDNA. The possibility that dogs originated in connection with the transition from hunter gathering to farming of rice (Bellwood, 2005) has been suggested, based on mtDNA indicating dogs to have originated approximately at this time (Pang et al., 2009). This would place the origin of dogs in Northern/Central ASY where the earliest evidence of rice cultivation has been found (Underhill, 1997; Bellwood, 2005). However, the highest Y-chromosomal diversity was found in Southw ASY, which was also the only region harbouring the full set of the principal mtDNA haplogroups (Pang et al., 2009). The southern range of wolves would define the southern limit for possible domestication of wolf, but the historical range of wolf in the region is not known. Thus, although the principal region of dog origins has probably been identified, many details remain to be studied. However, analyses based on denser sampling and application of the new generation of powerful DNA sequence analysis has the potential of producing a very detailed phylogeographic map of the region, promising a detailed picture of the first steps in dog origins.

Conclusion

With this study of Y-chromosome diversity among dogs worldwide, we present a second global dataset, in addition to mtDNA, for studies of dog origins. These two independently inherited genetic markers give strikingly similar pictures of dog phylogeography. Most importantly, both markers show that ∼50% of dog genetic diversity is shared in a universal gene pool, but whereas most regions harbour only these 50%, ASY has virtually the full range of genetic diversity from which the complete gene pools in other regions may have derived.

This offers strong evidence that domestication of wolf occurred primarily and possibly exclusively, in ASY. Both markers also indicate that a large number of wolves, probably several hundred, were domesticated, which suggests that taming of wolf was an important cultural trait in the related human populations. Subsequent hybridisation between dog and wolf seems to have occurred only rarely.

Studies of the archaeological record and autosomal SNP data have not indicated ASY to be the region of dog origins but, because of an almost complete lack of samples from ASY in these studies, evidence indicating ASY may have been overlooked. In the light of the Y-chromosomal and mtDNA data it is clear that comprehensive sampling from across the world, and especially ASY, is necessary for studies of early dog history.

Based on this knowledge, analyses of haplotypic and autosomal genome-wide markers on geographically dense sample collections and systematic archaeological investigations of canid material in neglected regions, can now be initiated. Hereby, elucidation of details, such as the more exact location(s) of dog origins in ASY, the possibility that independent domestication of wolf also occurred in regions other than ASY and the extent of crossbreeding of dog and wolf through history seems within reach.

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Sacks BN1,Mol Biol Evol. 2013 May;30(5):1103-18. doi: 10.1093/molbev/mst027. Epub 2013 Feb 13. Y chromosome analysis of dingoes and southeast asian village dogs suggests a neolithic continental expansion from Southeast Asia followed by multiple Austronesian dispersals.

Abstract

Dogs originated more than 14,000 BP, but the location(s) where they first arose is uncertain. The earliest archeological evidence of ancient dogs was discovered in Europe and the Middle East, some 5-7 millennia before that from Southeast Asia. However, mitochondrial DNA analyses suggest that most modern dogs derive from Southeast Asia, which has fueled the controversial hypothesis that dog domestication originated in this region despite the lack of supporting archeological evidence. We propose and investigate with Y chromosomes an alternative hypothesis for the proximate origins of dogs from Southeast Asia–a massive Neolithic expansion of dogs from this region that largely replaced more primitive dogs to the west and north. Previous attempts to test matrilineal findings with independent patrilineal markers have lacked the necessary genealogical resolution and mutation rate estimates. Here, we used Y chromosome genotypes, composed of 29 single-nucleotide polymorphism (SNPs) and 5 single tandem repeats (STRs), from 338 Australian dingoes, New Guinea singing dogs, and village dogs from Island Southeast Asia, along with modern European breed dogs, to estimate the evolutionary mutation rates of Y chromosome STRs based on calibration to the independently known age of the dingo population. Dingoes exhibited a unique haplogroup characterized by a single distinguishing SNP mutation and 14 STR haplotypes. The age of the European haplogroup was estimated to be only 1.7 times older than that of the dingo population, suggesting an origin during the Neolithic rather than the Paleolithic (as predicted by the Southeast Asian origins hypothesis). We hypothesize that isolation of Neolithic dogs from wolves in Southeast Asia was a key step accelerating their phenotypic transformation, enhancing their value in trade and as cargo, and enabling them to rapidly expand and replace more primitive dogs to the West. Our findings also suggest that dingoes could have arrived in Australia directly from Taiwan, independently of later dispersals of dogs through Thailand to Island Southeast Asia.

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The question of dog domestication origins is neither totally settled nor uncontroversial. Some believe the dog was domesticated more than once, and once in Europe/W Eurasian, and another in East Asia, see Grimm D., EVOLUTION. Dogs may have been domesticated more than onceScience. 2016 Jun 3;352(6290):1153-4. doi: 10.1126/science.352.6290.1153.

Franz LA et al., Genomic and archaeological evidence suggest a dual origin of domestic dogsScience. 2016 Jun 3;352(6290):1228-31. doi: 10.1126/science.aaf3161. Epub 2016 Jun 2.

The above analyses revealed “a deep split separating modern East Asian and Western Eurasian dogs. Surprisingly, the date of this divergence (~14,000 to 6400 years ago) occurs commensurate with, or several millennia after, the first appearance of dogs in Europe and East Asia. Additional analyses of ancient and modern mitochondrial DNA revealed a sharp discontinuity in haplotype frequencies in Europe. Combined, these results suggest that dogs may have been domesticated independently in Eastern and Western Eurasia from distinct wolf populations. East Eurasian dogs were then possibly transported to Europe with people, where they partially replaced European Paleolithic dogs.”

 

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