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ZOOLOGICAL SCIENCE 8: 639-651 (1991) <' 1991 ZoologicalSocietyofJapai REVIEW The Origin of Japanese Dogs and their Association with Japanese People Yuichi Tanabe1 Department of Animal Science and Technology, Faculty of Agriculture Gifu University. Yanagido, Gifu 501-11, Japan Pigeons (Columba livid), camels (Camerus bact- Short History of Domestication of Animals lianus, Camerus dromedarius), lamas {Lama gla- with Emphasis on Dogs ma), alpacas (Lama pacos), buffaloes (Bubalus Most relationships between man and the bubalus), honey bees (Apis mellifera. Apis cera- domesticated animals are commensalism, meaning na), silk worm moths (Bombix mori), Asian aclose association orunion between twospeciesof elephants (Elephas maximus), cats (Felis cattus), organisms, in which one is benefitted by the rela- guinea pigs (Caviaporcellus), geese (Anserdomes- tionship and the other is neither benefited nor ticus), ducks (Anasplatyrhinchos), msucovy ducks harmed, but it is not a parthnership. meaning that (Cairinamoschata), turkeys(Meleagrisgallopavo), in which both are mutually benefited, except in guinea fowls (Numida meleagris) and yaks (Bos two cases: that of the dog and the cat (see for gruniens) were domesticated in the prehistorical reviews: Mason [1] and Tanabe [2]). and early historical periods after the establishment Dogs (Canis familiaris) are the oldest domesti- of agriculture. Most of then were domesticated in cated animal in the preagricultural age, and were the Old World, except lamas, alpacas, guinea pigs. domesticated between 14,000 and 12,000 before muscovy ducks and turkeys, which were domesti- present (BP) [3]. However, the earliest archaeolo- cated in the New World [1, 2]. gically dated (ca. 35.000-38.000 BP) evidence for Mice (Mus musculus) and Norway rats (RattUS the presence ofdomesticated dogs comes from the norvegicus) encountered man in the early agri- Douara Cave near Palmyra in Syria [4]. Dogs are cultural age. and have been parasite animals for a believed to have derived solely from wolves (Canis long time. However, a large number ofthem have lupus) [5. 6. 7]. been domesticated and have been used as ex- Man also domesticated reindeers (Rangifer perimental animals in biology and medicine [2]. tarandus) in the early preagricultural age (15,000 In the historical age, a lew wild animals were BP). and sheep (Ovis dries), goats (Caprqa hir- domesticated; i.e. rabbits [OryctolagUS Cuniculus) cus). pigs {Sus domesticus) shortly before the for meat production in France, Japanese quail preagricultural age. Cattle [Bos taunts) and chick- (Coinmix COturnix japonicd) for egg production in ens (Gallus gallus domestica) were domesticated Japan, minks (Mustcla vison) and foxes (Vulpes shortly after the start ofagronomic agriculture (ca. vulpes) for lur production in U.S.A.. Canada and 10,000 BP) [1. 2]. l SSR [1. 2|. Interestingly, a few animals had been domesticated and became commensalism animal, but have Received May 29. 1991 Present address: School of Vetcrinar\ Medicine. been abandoned by man latei. TWO of examplesof Azabu Universtiy. Fuchinnhe. Sanamihara. Kanagawa them are African elephants (LoxodontQ afrit mus) 229, Japan and cheetas (Acinonyx jubotus) [1. 2|. 040 Y. Tanabe Although man has regarded animals around him breed (pedigreed): 229 Jindo dogs, and one Ko- as a source of food and raw materials, the domes- rean local population: 125 Chejudo dogs; (c) ten tication ofthe dogcontinued an exception, as man Japanese native breeds or varieties (pedigreed): and dog joined to form a hunting team in the 119 Hokkaido, 240 Akita, 108 Kai, 81 Kishu, 90 preagricultrual age. In this sense, the relationship Shikoku, 70 Akita Shiba, 206 Shinshu Shiba, 113 man and dog can be called partnership but not Mino Shiba, 65 San'in Shiba and Ryukyu (103 commensalism which is commonly observed be- Yanbaru, and 30 Ishigaki) dogs, and eight tween man and other domesticated animals [8]. Japanese local populations: Mie hunting dogs (30 Dogs always migrated with man since the in Shima and 19 inNanto), 83Tsushima, 40Iki, 45 ancient ages. The evidence suggests that it is Tanegashima, 38 Yakushima, 92 Amamioshima, possible to trace the route ofmigration ofman by 71 Okinawahonto and 20 Iriomotejima; (d) 144 tracing the route ofdog populations in the prehis- Taiwan native dogs and three Chinese origin toric ages. breeds (pedigreed): 20 Chin, 10 Chow Chow and 18 Pug; (e) 15 European breeds (pedigreed): 33 Shetland Sheepdogs, 73 Malteses, 16 Poodles, 22 Blood Protein Polymorphisms ofDogs Collies, 64 Pointers, 26 Boxers, 28 Yorkshire Findings of polymorphisms in blood proteins Terriers, 74 German Shepherds, 19 English Set- including enzymes (isozymes) in various demosti- ters, 20 Cooker Spaniels, 27 Pomeranians, 14 cated animals have enabled us to elucidate the Dalmatians, 20 Doberman Pinuschers, 18 Dach- genetic relationships of the breeds or populations shunds and 412 Beagles; (f) 3 Russian breeds of the animals. (pedigreed): 34 Laikas, 27 Middle Asian Sheep- Bloodsamplesweretakenbyusfromtheforeleg dogs and 27 Caucasian Sheepdogs; (g) 60 Bang- vein of 3,632 individual dogs including (a) 20 ladesh native dogs. Eskimo dogs (pedigreed); (b) one Korean native Blood was centrifuged at 3,000rpm for 10min. Table 1. Genetic variations in the 16 blood proteins or enzymes, and the made of inheritance. proteins or enzyme Locus Allele Reference Protein Plasma albumin (Alb) AlbF=Albs [12] Plasma postalbumin (Poa) PoaA=PoaB=Poac [13] Plasma postalbumin-3 (Poa-3) Poa-3A=Poa-3B [14] Plasma prealbumin-1 (Pa-1) Pa-lA=Pa-lB [14] Plasma transferrin (Tf) TfA=TfB=Tfc=TfD=TfE [12, 15] A Plasma pretransferrin (Ptf) Ptf >Ptf° [16] Erythrocyte hemoglabin (Hb) HbA=HbB [17] Enzyme Plasma alkaline phosphatase (Akp) AkpA=AkpB=Akpc [13] Plasma esterine resistant esterase (Es) EsA=EsB=Esc [18] Plasma leucine aminopeptidase (Lap) EapA=LapB [19] Erythrocyte acid phosphadase (Pac) PacF=Pacs [19] Erythrocyte esterase-2 (Es-2) Es-2s>Es-2F [13] Erythrocyte esterase-3 (Es-3) Es-3A=Es-3B [13] Erythrocyte glucose phosphate isomerase (GPI) GPIA=GPIB [21] Erythrocyte tetrazolium oxydase (To) ToA=ToB [22] Erythrocyte gangliside monooxygenase (Gmo) Gmo8>Gmoa [11] A=B indicates that A and B are codominant alleles. A>B indicates that A is a dominant allele and B is a recessive one. Origin of Japanese Dogs 641 The erythrocyte traction was washed twice with Prefecture. The Kai dog is a medium-sized breed, isotonic saline. The plasma and cell fractionswere body height being 40-50cm, originating from stored separately at —80°C until use. Horizontal Yamanashi Prefecture, and characterized by the starch gel electrophoresis for enzymatic proteins brindle coat color. The Kishu dog is a medium- [9], horizontal polyacrylamide gradient gel elec- sized breed, body height being46-55 cm, originat- trophoresis for non-enzymatic proteins [10], and ing from Wakayama Prefecture. The Shiba dog is thin layer chromatography for ganglioside a small-sized breed, body height being 35-41 cm, monooxygenase (11] were used to detect elec- and consisting four local varities, i.e. Shinshu trophoretic and biochemical variations of proteins originating from Nagano Prefecture and a major in plasma and erythrocytes. variety spreading all over Japan; San'in is a minor Genetic variations were observed in six loci one living in Tottori and Shimane Prefectures. composed of seven non-enzymatic proteins: plas- Mino is a minorone, living in Gifu Prefecture, and ma albumin (Alb), plasma postalbumin (Poa), Akitaoriginaing mainlyeastern partsofJapan and plsma postalbumin-3 (Poa-3). plasma prealbumin- belongingtoShiba-Inu Preservation Association at 1 (Pa-1). plasma transferrin (Tf), plasma pretrans- Omagari in Akita Prefecture, andcharacterized by ferrin (Ptf) and hemoglobin (Hb), and nine en- the very shallow-stopped face. The Shikoku is a zymatic proteins: plasma alkaline phosphatasa medium-sized breed, body height being 46-52cm, (Akp), plasmaeserine resistantesterase (Es), plas- originating Kochi Prefecture in Shikoku Island. ma leucine aminopeptidase {Lap), erythrocyte The Ryukyu dog is a medium-sized breeds, origi- acid phosphatase (Pac). erythrocyte esterase-2 naitng from Nago-shi and Yanbaru district in (Es-2). erythrocyte esterase-3 (Es-3), erythrocyte northern Okinawahonto and a similar one is in glucose phosphate isomerase (G/7), erythrocyte Ishigaki Island, and both are characterized by the tetrazolium oxidase (To) and ganglioside monoox- brindle coat color. There are eight local popula- ygenase {Gmo). On the other hand, no genetic tions of indegenous dogs in Japan. Five of them variations were found at 11 loci controlling three are living in the Ryukyu or Nansei Islands: Tane- non-enzymatic proteins: plasma postalbumin-2 gashima, Yakushima, Amamioshima, Okinawa- (Poa-2). plasma prealbumin-2 (Pa-2) and plasma honto (middle and southern regions) and slow-a2 macroglobulin (a2) and eight enzymatic Iriomotejima. Two of them are living in the two proteins: plasma amylase (Amy), plasma eterase- islands existing between Japan and Korea: Iki and Easl (Es-f). erythrocyte adenylate kinase (Ak), Tsushima. The final two are living in the Shima erythrocyte esterase-fast (Cell-Es-f), erythrocyte peninsula and Nanto-machi in the south-east coast glucose-6-phosphate dehydrogenase (G-6-PD), of the Kishu peninshula, and are called Mic hunt- erythrocyte lactate dehydrogenase-A and -B ing dogs (Shima and Nanto). (LDH-A and LDH-B) and erythrocyte leucine There are four indigenous dog populations in aminopeptidase (Cell-Lap). The mode of inheri- the mountain area of Taiwan [25]; Atyl (north), tanse of all the polymorphisms loci are given in Bunun (middle), Rukai (south) and Ami (east). Table 1. The dogs were named after the names of tribes living in the area. Data from these dog populations were combined, because the genetic differ- Description of Native Dog Breeds and Populations ences among the populations were small. in Japan and Its Adjacent Areas The Jindo dog is a medium-sized breed, and is In Japan, there are 1 1 indigenous dog breeds or the only one registered as a Korean native bleed. varieties (pedigreed) [23, 24]: the Hokkaido dog is originating from Jindo Island We took blood a medium-sized breed, body height being 40-55 samples from 210 pedigreed clogs on Jindo Island cm. orignating from Hokkaido Island, and used to and 19 pedigreed ones in Seoul [25]. then be called the Ainu dog because it was kept by indigenous dog populations in Chejudo I! rid Ainu. The Akita dog is a large-sized breed, body [25]. We took blood samples of 1 kin logs height being 58-70cm. originating from Akita (pedigreed) in Obihiro Zoo and ad reas, 64: Y. Tanabe and also from the indigenous dogs in Bangladesh Genetic Relationships ofDogs with Emphasis [26, 27]. on Asian and Japanese Dogs The blood samples from three Chinese origin dog breeds (the Chow Chow, the Chin and the Thegeneticrelationshipsamongthedogbreeds, Pug; all pedigreed), and 15 European dog breeds with special reference to Asian dog breeds includ- (pedigreed) were collected from various institu- ing Japanese dog breeds, were studied by bioche- tions. Universities and veterinary hospitals in mical polymophisms of the blood detected by Gifu, Nagoya and Tokyo in Japan. The blood electrophoretic and chemical analyses. The inten- samples of three Russian dog breeds (pedigreed) tion was elucidate the origin of Japanese native were collected in Novosibirsk, USSR. dogs with an emphasis on their migration routes European Eskimo Russian/ dogs dog dogs f O Akita dog Bangladesh China / native origin/ dogs dogs f Ryukyu dog n [v sJ (Ishigaki Fig. 1. Geographical distribution ofdog erythrocyte hemoglobin (Hb) variants in Japan and its adjacent areas. ) Origin of Japanese Dogs 643 and their association with Japanese people [12.14. peninsula into the Japanese Islands. A similar 24. 28, 29]. tendency was found in the genes of Gmo. Gmo8 The most prominent differences of gene fre- was also found only in Asian breeds or popula- quenc\ among the dog breeds or populations were tions, but not in European breeds and Russian obsereved in Hb and Gmo variations. HbA was breeds. Distribution of Gmo alleles among the found only in Asian breedsorpopulations, but not Asiandogbreedsorpopulations isshown in Figure in European breeds and Russian breeds. Distribu- 2. This Figure also shows the gene flow of Gmo* tion of Hb alleles among the Asian dog breeds or from the Korean peninsula into the Japanese Is- populations is shown in Figure 1. The data clearly land except Hokkaido. show the sene flow of HbA from the Korean Poa-3A is a predominant allele in the European European Eskimo dogs dog © (5 Bangladesh Chinese native origin dogs dogs Ryukyu dog Ishigaki ( Fig. 2. Geographical distribution of dog erythrocyte glycolipfd (Gmo) variants in Japan and it etdjacenl areas 644 Y. Tanabe breeds, but the frequency of Poa-3B is higher in An apperent cline in the Ptflocus is observed in the Asian breeds or populations than the Euro- dog breeds or populations. PtfA predominates in pean breeds. Distribution of Poa-3 alleles among the Eskimo, the Russian, the Europian, the the Asian dog breeds or populations is shown in Chinese origin andtheJindo (Korean) dogs, andis Figure 3. This Figure also shows the gene flow of intermediate in most of the Japanese dogs in Poa-3B from the Korean peninsula into the Honshu, but low in the Ryukyu, the Iriomote and Japanese islands. Similar tendencies were observ- the Hokkaido dogs in Japan, and the Bangladesh ed in the gene frequencies in Poa, Alb, Tf, Es, native dogs. Distribution ofPtfalleles among the Es-2, GPI, and Pacpolymorphismsamongthedog AsiandogbreedspopulationsisshowninFigure4. breeds or populations examined in this study. In orderto summarize dataofallele frequencies European Eskimo Russian/ dogs dog dogs f ® Hokkaido dog (3 Bangladesh Chinese ), Akita dog native origin/ dogs dogs r Shiba dog (Akita) Kai dog Mae hunting dogs Shima) ( Mie hunting dogs Nanto) ( Fig. 3. Geographical distribution ofdog plasma postalbumin-3 (Poa-3) variants in Japan and its adjacent areas. Origin of Japanese Does 645 European dogs Eskimo dog Russian dogs Hokkaido dog Akita dog Kai dog Mie hunting dogs (Nantocho] egashima dogs V 7yakushima dogs imamioshima dogs Okinawa dogs h/ r i . 3^Ryukyu dog C^p. C J ^& ) Taiwan native dogs Fig. 4. Geographical distribution of dog plasma pretransferrin (/'//) variants in Japan and its adjacent areas over variable loci, a principal component analysis pupulations of the Hokkaido, the K\uk\ti lan ( (PCA) based on the variance-covanance matrix barn and Ishigaki). the Inomote and the Yakushi- computed from the frequencies was conducted ma dons, and a close relationship smong the ko [Methodology references: 30, 31]. rean native breed (the Jmdo) or population (the A scatter diagram of relative positions of the 4b (hejlldo), and some ot Japanese native breeds and dog breeds or populations plotted on the basis <>t poulations such as the San'm Shiba. the Akita. the the 1st and 2nd principal component scores is Ntie hunting dogs m Shima and the Tsushima dogs. illustrated in Figure 5. These two components Further, there is a close relationship amoi account for 44.9% of the total variance. This Taiwan native dogs, the Chinese origii figure clearly show the existence of the two close- Chin, the Pug and the (how Chov relationships among some Japanese breeds or MinO-Shiba and the Sliikokn l! I .:ii be postulated 646 Y. Tanabe — 3 O i/) •EH CCO —•--H TOJ rgr-1 -•Hj-OrCO^^JTô"ÔJ'ae-j«HnD'1O—c3iur-rDcoIH/'rl>^rO-'iu_or^ccc=5Hj-j1')-U-rgo^-£a—wJ1ceH/1Mn'iJCso-J~—OD-Cc3«<3=rH>H'o-uc-i-J-—^,cOH=-?Ho0n:'^xi-J^P'O)tHaC3OKom^j—x'roCCEiTiacn:it>-a--,ErROrQ3*aJCnxiH,jE,-:ODm6ECrOiwOh-0TxOioCmCS-^:'OocHoEa1-tOnot-D)J»aHudi47-D:O-—rJc>cawCCHDjJni-tOccw-:r-ÔaCCrHhJTct>-,-^nonHrHrex3oW3Coi>>D/iir-XiiD>>3Cero!Z—7,r>^xa>o-r—HJa:c>co3Hi^mr,>rcCKc--Tj-Ocu>rHJhuaa!'o-TOcCH3anPxJTCeOo-))=JHnxn-X-i:rir1C>oCHu!anOj0oJ-OuHtijHcimCV/lJj--HCcO^XorJTxcE<CaoCmM):ooJjUZpHQaraH0)i*xTtaJmaCoOrCcJ:DdCJoji-vU^--ei^0hc^rVc-Hi-jj<'i--Enj^mrrc-UoaHxijw:-i<qc^CC^jjaHH:-)mracoUOMHnj CDHJxUO>os:=jE-J_touccrWCc3hcnjoajO-HHHoOia--XroccEhjoiiIrrcia3U/a-O)OOa.oO-.t^<Weudwn~r-tmirur«monm3h-ii3'qOm-.-T_<mrCiHh)cDa-(-îHrCa3"Q°°£Mc5f03-- r-^\n^^Lôr^c^(7lcpr-NnvLnoôoÔr-Nnû^vD^cooô^-Mr^^^^rlvo^cÔlO^-OJ^^l^vo•5 ^^r-r-r-r-r-^r-r-rvirvirviN^NiNrviNrNrnrinnnriririnnv^^vvvvn. Cn O TJ in v3* V.. i!i rOCu3oaoJ TxQUQ3)JJ «1Nt—? .£°tCc2/O>23 \coeCpOg 'w qj co — -G <u Xi fl ^j "O *>* £ill O £ g rS \ Q) iQnJ ii -°a _§1o nni QJ ' <u X) i O X) co .Ca - wa Oc/3 GC ClD-X CL, <U "3 T3 £ p* <u c m. <4o-H cCOl 6 Origin of Japanese Dogs 647 that there were at least two waves ofthe gene flow the Russian dog breeds, i.e. the Laika and the of dogs into Japan: the first was from southeast Caucasian Sheepdog. Asia through Ryukyu and orTaiwan to the whole To simplify the data, dog breeds or populations of the Japanese islands including Hokkaido, and used in the study were placed in seven groups: 1. the second was from the Korean peninsula to the Japanese native dogs (1, 556 dogs). 2. Korean Japanese main islands except Hokkaido. native dogs (354 dogs). 3. Taiwan native dogs (144 It is interesting that a close relationship alsowas dogs). 4. Bangladesh native dogs (60 dogs), 5. observed between the Hokkaido dog (the Ainu Chinese origin dogs (64 dogs), 6. European dogs dog), which lives in the far-northen portion of (953 dogs), 7. Russian dogs (93 dogs) and S. Japan, and the Ryukyu dog. which lives in the Eskimo dogs (20 dogs). The relative positions of far-southern portion ofJapan. The gene constitu- the eight dog breed groups were defined by the tion ofthe Hokkaido dog is different from most of first (Zl), second (Z2) and third (Z3) largest the other Japanese dog breeds or populations principal components of distance matrix based on except some dogs groups including the Ryukyu, variance-covariance analysis (Figure 6). These the Iriomote. and the Yakushima dogs. Forth- three components account for 87.2% of the total ermore. aclose relationshipwasobserved between variance. In Figure 6, it is clear that the Japanese the gene constitution of the Chejudo dogs and native dogs are located between acombined group someJapanese doggroupssuch asthe San'in Shiba of the Taiwan native dogs and the Chinese origin dog. the Tsushima dogs, and the Akita dog. The dogs, and agroupofthe Korean nativedogs, while position ofthe Eskimo dogis far from all the other the position ofthe European dogs and the Russian dogs, but some close relationship was observed to dogs is also nearer, whereas those of the Bang- .Japanese native dogs 1 2.Korean native dogs Z3(16.1%) 3.Taiwan native dogs 0.140 4. Bangladesh native dogs 5.Chinese origin dogs 6 . European dogs 7.Russian dogs .Eskimo dog *o ; Fig. 6. Relative position of 8 dog breed groups defined by the first three (Z1-Z3) principal COfll| the distance matrix based on variance-covariance analysis of izcne frequents at [6 polymorphic parentheses represent the contribution to the total variation. MS Y. Tanabe ladesh native dogs and of the Eskimo dog are farther from the Japanese native dogs. From the results descrived above, it is postulated that the Hokkaido (Ainu) and the Ryukyu dog breeds are descended from an old type of the Japanese dog which was brought 10,000-12,000 years ago to Japan by the Jomonese who came from southeast Asia through Ryukyu islands. The other Japanese native breeds are descendants of the hybrid between the old type of the Japanese dogs and the Korean origin dogs which were brought 1,700-2,300 years ago by Yayoi migrants who came though the Korean peninsula. The genetic distance between the Japanese native dogs and the Korean native dogs is farther than that between the Japanese native dogs and a combined group ofthe Taiwannative dogsandthe Chinese origin dogs, suggesting that the numbers of an old types of the Japanese dog which was of southern origin, were larger than those of new comers from the Korean peninsula. Cranial and Other External Studies on Dogs in Japan and Its Adjacent Areas Archaeological evidence suggested that the cul- Fig. 7. Skulls of dogs in ancient age in Japan. Top to tuer of dog keeping, which was initiated 9,500 down, a skull at Shuridai-shell mound in Chiba-shi, yearsagoattheearlieststageoftheJomonperiod, ccah.o3i,n5I0w0aBtPe,prtehfeeclattuereJ,ocmao3n,5p0e0riBoPd,; attheHalamtaeiJzoummoin- was brought into Japan from South China or period; at Chibachihigashi Kamakura-shi, ca. 800 somewhereelseinsouthernpartsofEastAsia, and BP (AD 1,200); Ibid., Courtesy of Mr. Hiromasa the Yayoi culture beginning 2,300 years ago, Kaneko [34]. brought another group or groups of dogs into Japan through the Korean peninsula [32, 33]. veryshallowstops [37], indicatingthe introduction A remarkable difference was observed in skull ofanewtype dogwith deep stops into the Kyushu morphology between the dogs in the late Jomon districtofJapan fromthe Koreanpeninsuladuring period (ca. 3,500 years ago) and the dogs in the the Yayoi period. Middle age (13th Century) in Japan [34]. The There are breed differences in the incidence of former had flatorveryshallowstops and the latter tongue spots. The incidence is about 30% in the had deep stops (Figure7). Dogskullsfoundin the Taiwan native dogs and 23.3% in the Ryukyu dog Kuwanae remains in Oita Prefecture in Kyushu in Ishigaki, while is very low in the Jindo (1.9%) (aging ca. 2,000 years, the middle of the Yayoi and the Chejudo (2.4%) dogs, and the values of perid) had deep stops [35] and showed a close Japanese native breeds varied between those of affinity to dog skulls found in the Uenongigiseori- Taiwan and Korean dogs, i.e. the Hokkaido: pohang remains in North Korea (aging 2,500- 88.5%, the Akita: 1.4%, the Kai: 35.5%, the 3,000years). Theseskullshaddeepstops [36], and Kishu: 4.1%, the Shinshu Shiba: 0.7%, the San'in were quite differentfrom dogskullsfoundinmany Shiba: 64.5%, the Mino Shiba: 19.1%, and the shell mounds in the Jomon period (2,500-10,000 Shikoku: 21.8% [23, 25, 38]. years ago), where the skulls of the dog had flat or It can be concluded that the main body of