Canine Domestication May Have Begun 30,000 or More Years Ago

Canine domestication is only certain after the Last Glacial Maximum, though the increasing evidence of variant wolves living close to settlements of Eurasian hunter-gatherers in the Upper Paleolithic argues that it may have already begun 30,000 or more years ago.  This proximity of species may have led to the sort of self-domestication described by the Coppingers (2001), though the size of the game may suggest that the wolves were initially more determined to get close to the hunt than the camp.

Wolf (Dog?) in Font-de-Gaume Cave, Magdalenian Culture (painting by Breuil, 1910)

More data will be necessary to say for sure that the morphological changes of wolves living near human habitations in the Aurignacian, as described by Germonpre (2009, 2012, and 2013), continued until there were dogs.  Even if continuity can be established, there very likely was a significant bottleneck before or in the Last Glacial Maximum, and perhaps migration of humans and canids out of areas where glaciation reduced or eliminated hunting opportunities.  These migrations may explain the first bifurcations of an initially domesticated wolf population. Alternatively, the initial domestication may have remained incomplete and disappeared during the Last Glacial Maximum (Ovodov et al. 2011).

The conservative and still more accepted position is that domestication began in increasingly sedentary human settlements after the Last Glacial Maximum, perhaps in East Asia about 16,000 years ago as argued by Savolainen et al. (2002), though it could also have occurred in Southeast Asia (Brown et al. 2011), the Middle East (vonHoldt et al. 2010), or even Europe (Verginelli et al. 2005; Wayne and vonHoldt 2012).  It may have begun in several places more or less simultaneously (vonHoldt et al.; Pionnier-Capitan et al. (2011)), and there may have been different functions for dogs in the different cultures where domestication began (Gray et al. 2010; Driscoll and MacDonald (2010)).

Germonpre et al. (2012), conceding that dogs after the Ice Age are smaller than what they call Upper Paleolithic dogs, suggest that once some of the larger game began to disappear, smaller dogs would have become more useful.  They acknowledge that “it is difficult to ascertain at the moment whether the small prehistoric dogs were descending from a European Palaeolithic stock of large dogs, which finds its origin in the Aurignacian, through selection for a smaller body size, or were introduced from elsewhere.”  Thus, though arguing that there was a long period of domestication before the Last Glacial Maximum, they leave open the possibility of subsequent domestication events. 

ARCHEOLOGY

Eurasian Sites Discussed in Text

Because of the specifically identified locations involved in excavations, and the generally more specific dating, it is easiest to begin with the lines of archeological research before describing the genetics research and then attempting a synthesis.  The table at the end of the blog combines the archeological and genetic evidence into a single timeline.  

The first map shows the locations of most of the sites that will be discussed. 

Kostenki, 40,000 Years Ago 

Mietje Germonpre, Martina Laznickova-Galetova, and Mikhail Sablin, in a paper published in the Journal of Archaeological Science in January 2012, compare the associations of wolves with humans over three periods, beginning with the early Upper Paleolithic site at Kostenki on the River Don, dated  between 41,000 and 38,500 years ago.  The most common bones found at the site are those of the broad-toed horse (Equus latipes), but there are also bones of bison, hare, arctic fox, mammoth, and red deer.  Bones of wolves were found.  (Hoffecker et al. 2009)  Holliday et al. (2007) argue for the presence of anatomically modern humans in the area, probably prior to 40,000 years ago.  Neanderthal occupation has not been ruled out.  Germonpre and her colleagues saw this site as a sort of base line, a point where there is no indication of cooperation or domestication, though the two species are close and hunt the same large mammals. 

Goyet Cave, 36,000 Years Ago

A skull found in the Goyet Cave of Belgium was identified by Germonpre et al. (2009) as coming from a Paleolithic dog about 36,000 years ago, putting it in the Aurignacian cultural period. (Radiocarbon dates of c. 32,000 BP were published in Germonpre (2012), resulting in a calibrated age of at least 36,000.)

mtDNA analysis of the skull, and of two other skulls identified as Paleolithic dogs from the Ukraine (at Mezin and Mezhirich, dating from the Epigravettian cultural period) “yielded unique DNA sequences, indicating that the ancient Belgian large canids carried a substantial amount of genetic diversity.” The researchers concluded that the mtDNA analysis indicated that the three dogs “do not form a homogenous genetic group.”  They cite the argument of Lindblad-Toh et al. (2005) that an ancient genetic bottleneck accompanying the domestication of dogs occurred around 27,000 years ago, eliminating much of this early diversity.  (Genetic diversity was also found in fossil canids in Italy by Verginelli et al. (2005), including one canid found at the Palidoro Upper Paleolithic rock shelter in Latium.) 

Nevertheless, all the Paleolithic dogs showed considerable uniformity in skull shape, and this “skull morphology seems to have remained stable” with dogs from that point forward. “[A]ncient dog skulls have shorter and broader snouts, wider palates, and wider braincases than wolf skulls.”  (Germonpre et al. 2012).  “Their skull size suggests that these first dogs were large animals, as large as recent large dog breeds….” Germonpre et al. (2009) hypothesized that “changes in dog morphology compared to wolf morphology appeared rather abruptly, that they were linked to the effects of domestication and that these changes became fixed in the dog population.”  Thus, although there was genetic diversity, changes in skull shape was universal to the domestication process.  (Curiously, the same presence of shorter jaws and wider skulls is found in Belyaev’s artificially domesticated silver foxes.)

Mammoth Tracing, Font-de-Gaume Cave, with Structure Superimposed

The Goyet Cave canid skull was found in a side gallery where there were also remains of mammoth, lynx, and red deer.  The large canids found in the cave preyed primarily on horse and large bovids.  Although the researchers, only “tentatively propose that the domestication of the dog had already begun in the Aurignacian,” they argue that the dogs may have already had significant functions for humans.  “They may have been used for helping with the tracking, hunting or transport of large ‘ice-age’ game, possibly mammoths on the Russian Plain  … or used as pack animals….”  The Russian Plain argument presumably refers to the dogs identified at Mezin and Mezhirich.  Although stated with caution, this rather too easily projects more recent functions into the Aurignacian.  Tracking is certainly likely, but use of the animals for transport seems to posit rather too sophisticated a dog culture for such an early phase in the domestication process. 

As to why genetic studies generally do not place domestication as far back as the Aurignacian, Germonpre et al. state:

“Since dogs were domesticated from gray wolves, ultimately the first dogs would have carried a wolf-like genetic sequence, and hence will be not identifiable genetically as the first dogs. Only after isolated breeding, it is possible that certain genotypes in the Palaeolithic dogs drifted to high frequencies and might therefore be distinguishable from those of the source wolf population. Thus one would only expect to see a differentiation of dogs and wolves after several thousands of years due to the bottleneck caused by selective breeding during early domestication. At the same time certain (e.g. morphological) traits were probably expressed and selected for, or just arose by drift. After this initial phase of domestication a relaxation of constraints occurred. Wolves after the domestication (i.e. dogs) were insulated from the full force of negative selection because humans cared for them, e.g. providing food and physical protection – therefore (slightly) disadvantageous traits could still survive and produce offspring. These individuals in their natural environment would probably not have contributed to the next generation’s gene pool. Later, exponential population growth increased genetic diversity to the high levels that are observed in dogs today.”

Germonpre’s 2009 paper was criticized by Morey (2010), who said that “in the absence of a sound demonstration of the accuracy of their taxonomic inferences, I hold this as a markedly unconvincing case that dog domestication occurred that early….”  Crockford and Kuzmin (2012) quickly jumped on both papers on which Germonpre was the lead author (2009 and 2012) and found serious deficiencies in the conclusions of those studies that Paleolithic dogs were found at the sites.  They argued that “more work needs to be done to understand the biological mechanisms involved in wolf domestication.”  
 

Altai Mountains, 33,000 Years Ago

Ovodov et al. (2011) describe what they call a “33,000-year-old incipient dog from the Altai Mountains of Siberia.”  (Radocarbon dating placed the animal between 29,950 and 27,850 BP, with calibrated ages of c. 33,500-33,000 BP.) The skull was found in the Razboinichya (Bandit’s) Cave in southern Siberia, which is presently 90 meters long, up to 15 meters high near the entrance and even higher further back. Although charcoal was found, the researchers believe “the chamber was primarily used in antiquity by hyenas as a den” because the remains of at least 137 individual hyenas were found, along with deposits of hyena coprolites (fossilized feces).

The wolf skull measurements are similar to those of Neolithic and later dogs, though the teeth are not crowded as appears in Neolithic dogs but closer in size to wolf teeth.  The researchers concluded that they were looking at an “incipient” dog, rather than an aberrant wolf.  Noting that confirmed dogs do not appear until the Holocene (14,000 to 11,500 years before present), they argued that “the lineage represented by the incipient dog from Razboinichya Cave did not survive the LGM [Last Glacial Maximum, c. 26,500 to 19,000 years before present].”  The researchers also considered a similar animal from the Goyet Cave, to be discussed next, to be an incipient dog whose lineage did not survive. 

Citing archeological research on human occupation of the area in the Altai Mountains where the skull was found, Ovodov et al. state that the humans “appear to have been relatively sedentary hunter-gatherers who stayed in one place for many months at a time.”  Although human occupation continued in the area through the Last Glacial Maximum, this was apparently “without dogs, perhaps because humans in northern Eurasia became somewhat less sedentary. Not until the Ice Age began to wane did the human settlement patterns conducive to domestication of wolves become common again, i.e., year-round sedentism or sedentary hunter-gathering.” 

Russia and Siberia, showing Kostenki and Altai Mountains

Curiously, though this might be seen as the second step in the Paleolithic domestication process described by Germonpre in the following sections of this analysis, Germnonpre herself has placed some doubt on the significance of the Razboinichya Cave canid.  Responding to methodological and other criticisms from two of Ovodov’s co-authors, Susan Crockford and Yaroslav Kuzmin, Germonpre et al. (2013) noted that this canid has “only about 10% chance of actually belonging to the European Palaeolithic group” and that it may have “another origin.”  As indicated on the second map, the Siberian cave is a considerable distance from any of the other early Eurasian sites. 

Ornamentation in the Aurignacian

Germonpre refers to one area of research that may provide evidence for a changing relationship between humans and dogs in the Aurignacian.  Perforated canines from foxes and wolves were used for adornment at the Avdeevo site, dating from about 21,000 years ago, as were other modified bones and imitations of canid bones carved out of mammoth ivory (Gvozdover 1995; Germonpre 2009).  Belgian Aurignacian sites have also yielded wolf (dog?) teeth used as personal ornamentation. Not all cultures of the period used wolf teeth for ornamentation, according to Vanhaeren and d’Errico (2006).  These researchers argued that this distinction indicated the presence of different cultures in the Aurignacian: 

“[A]lmost all the mammal species (fox, wolf, horse, ibex, bovid, bear, lion, hyena) that provided teeth used to manufacture personal ornaments in Germany, Belgium and the southwest of France were also available in southeastern France, Italy, Greece, Mediterranean Spain, and Austria, as demonstrated by the presence of these animals at the Aurignacian sites from these areas.  Yet they were not used as beads.”  See also Cartmill and Smith (2009), noting that using bones and beads for personal ornamentation, but not seashells, may have begun with Neanderthals and could have continued among modern humans who had contact with Neanderthals.

Randall White (2003) disputes the claim as to “regionally distinct configurations of personal ornaments corresponding to geographically and linguistically distinct ethnic units,” saying that such “geographic units are not nearly as clear in the ethnographic record as one would like.”  White does, however, find cultural significance in the choice if which teeth are used for ornamentation:

“The animals whose teeth are worn are not those whose meat is consumed.  Phrased another way, the consumed fauna and the displayed fauna are almost mutually exclusive.  This implies that the animals behind the parts transformed into ornaments are construed in terms that are largely of the collective symbolic imagination.” 

None of the researchers working on personal ornamentation mention any possibility that the wolves whose teeth were used as ornaments may have been among those living close to human encampments.

Piedmosti, 27,000 Years Ago

In 1994, Benecke argued that the Piedmosti site in the Czech Republic indicated wolf domestication based on tooth crowding in mandibles, suggesting an early stage of domestication.  Germonpre et al. (2012) conducted a detailed analysis of the large canid skulls from this site and concluded that they can be identified as Paleolithic dogs.  The occupations “took place during the warmer episodes of the Pleniglacial that preceded the last glacial maximum,” perhaps between 26,000 and 27,000 years before the present. 

Reindeer in Font-de-Gaume Cave (painting by Breuil, 1910)

The people at the site hunted mammoth, horse, bison, and reindeer.  Curiously, large canids are the second most abundant group, represented by at least 103 individuals.  One complete skeleton of a dog or small wolf was found in the human burial zone, and in another zone of the site, seven or eight complete wolf skeletons were uncovered, but the skulls were broken.  The animals were likely eaten, at least on occasion. Another Gravettian site in the Czech Republic produced a wolf vertebra with cut marks suggesting the animal was dismembered or filleted (Svoboda et al. 2011). 

Germonpre et al. argue that “the domestication that started during the Aurignacian was still in process in the Gravettian.”  They repeat their earlier suggestion for sophisticated functions already existing for the dogs:

“[T]he presence of large dogs at Piedmostí and the Epigravettian mammoth sites suggests that these dogs were useful as beasts of burden for the hauling of meat, bones and tusks from mammoth kill sites and of firewood, and to help with the transport of equipment, limiting the carrying costs of the Piedmostí people. Such large animals would require a lot of food. Given that mammoth meat seemed to have been the staple food at Piedmostí, enough surplus food would have been available to feed the dogs.”

They remark on the “large frequency (40%) of perforated neurocrania” (something also found at Eliseevichi, discussed below).  Although this may be to eat the brain of the animal, it could also have ritual significance: 

“The fact that the same phenomena are found circumpolar testifies that these ritual practices are both common and widespread, and date from a much earlier period. In light of this, we may surmise with some confidence that humans perforated the canid skulls at Piedmostí as part of a ritual performance.”

Another possible indication of ritual involvement with these early dogs was the presence of a bone inserted inside the mouth of a dog, probably after the dog died. These factors “hint at a specific relationship between humans and large canids, including the possibility of the existence of a wolf/dog ritual that could be connected to the sending of souls.”

Other Sites

In the deepest part of the Chauvet Cave in France, a track of canid footprints was associated with those of a child…. Torch wipes made by this child were dated about 26,000 years ago.  Based on the short length of medial fingers in the footprints the canid track was interpreted as being made by a large dog.”  (Germonpre et al., 2009)  Nevertheless, the footprints could also be those of a captive wolf.

A Russian site at Eliseevichi, from about 17,000 years ago, yielded a large number of mammoth bones among the food debris of the site.  Reindeer and arctic fox were also common.  Sablin and Khlopachev (2002) noted that since wolves and humans were competing for the same food, “it is not difficult to surmise how an alliance could have been formed between them.”  These authors referred to their canid find as one of the earliest Ice Age dogs.  They argue:

“It seems probable that humans tamed wolf pups in many parts of the world and therefore that several subspecies of wolf contributed to the ancestry of the dog. We suggest that the specimens of dogs reported here were domesticated in situ from local northern wolves.”

Artistic Representations in the Magdalenian, 17,000 to 11,000 Years Ago

Canids are infrequent in early Eurasian rock art, though a polychrome painting of a wolf in the Font-de-Gaume cave in southwestern France has been dated to the Magdalenian culture, between 17,000 and 11,000 years ago.  Animals do not usually appear in rock art without having a function to the community of the artist, though the function may be impossible to fathom.  Although this early depiction of a wolf could indicate that for the inhabitants of this particular area of Paleolithic France, wolves could be viewed as food, this and other paintings on the wall of the cave could also be the earliest known depictions of dogs.  Although Abbé Breuil made watercolors of the paintings at a time when they were better preserved than they are now, he apparently sought to capture the essence of the paintings, rather than depicting them precisely as he saw them  (Eshleman 2009).

It is appropriate to note that the artists who painted the cave walls likely did not live in the cave.  One painting of a bison includes superimposed depictions of buildings, perhaps communal huts.  Another shows a structure superimposed on a mammoth.

GENETICS

In 1997, a team of scientists that included Carles Vila, Peter Savolainen, and Robert Wayne, analyzed canine mitochondrial DNA and concluded that their genetic evidence “suggested that dogs originated more than 100,000 years before the present.”  More specifically, they stated that “dogs could have originated as much as 135,000 years ago.”  They acknowledged that their “estimates may be inflated by unobserved multiple substitutions at hypervariable sites,” and said that sequence divergence in one clade “clearly implies an origin more ancient than the 14,000 years before the present suggested by the archaeological record.”  Further:

Bison, Habitations Superimposed, Font-de-Gaume Cave (painting by Breuil, 1910)

“To explain the discrepancy in dates, we hypothesize that early domestic dogs may not have been morphologically distinct from their wild relatives. Conceivably, the change around 10,000 to 15,000 years ago from nomadic hunter-gatherer societies to more sedentary agricultural population centers may have imposed new selective regimes on dogs that resulted in marked phenotypic divergence from wild wolves.” 

Verginelli et al. (2005) agree, saying: “[G]enetic separation between dogs and wolves is likely to have occurred only after the Neolithic agropastoral revolution (~8,000 YA) that resulted in incompatibility between wolves and humans because of the presence of livestock…” This group suggests that “Late Glacial/Early Holocene wolf populations of the West Eurasian steppes (that stretched over South-Eastern Europe and West Asia) contributed to the origins of the dog.”  They also indicate that the genetic data suggests “multiple independent Asian and European domestication events.”

Although Vila et al. (1997) may be the most widely cited canine genetics paper, many if not most of the contributors have not adhered to the early dating of domestication.

Divergence Analysis Places Separation 30,000 Years Ago

Skoglund et al. (2010), analyzing genetic divergence between dogs and wolves, calculated a dog-wolf divergence time of as recent as 10,000 years ago without gene flow between dogs and wolves.  They argued that this was too recent because “making inferences based on a model with complete isolation of dogs and wolves might underestimate divergence times.”   Taking into account a low level of gene flow, therefore, they pushed the divergence point back to 30,000 years ago.  This finding was rather tentative, however, given that population sizes and bottlenecking events could move the date one way or the other. 

This team considered divergence periods for separate wolf populations from China, India, Spain, and Alaska.  Curiously, they found Indian wolves closest to dogs, which is hard to correlate with some other studies (See Sharma et al. (2003), finding “local ‘pariah’ dog breeds were brought into the Himalayas and peninsular India by humans and were not domesticated independently” from Indian wolves; Li and Zhang (2012), finding Tibetan Mastiffs closer to dogs from East Asia).  Skoglund et al. favor the position that Middle Eastern wolves contributed “the major part of the ancestry of modern dogs,” because of their finding of closest proximity of Indian wolves and dogs.  This conclusion seems at present an unwarranted leap. 

Considerable caution must be exercised in trying to gather hard dates from such research.  As Vila et al. note in discussing backcrossing:

“[O]ur simulations suggest that the contribution of the ancestral species to the diversity of our domesticates could have gone far beyond the initial domestication events…. Unfortunately, the difficulties in modeling all of the factors that could affect the role of backcrosses (including the degree and time of overlap between the distribution ranges of the domestic and wild taxa or the rate of backcrossing) hinder an estimation of their frequency.”

East Asia Locus

In 2002, Peter Savolainen and his colleagues stunned the world of canine research by arguing that the locus of canine domestication was East Asia, and that this occurred about 16,000 years ago, a position they have bolstered a number of times since (Pang et al. 2009; Klutsch and Savolainen 2011; Ding et al. 2012).  In defending his East Asian argument, Savolainen argued that further research may move most of the inconsistent archeological finds into the category of aberrant wolves (Klutsch and Savolainen).

In 2009, Boyko et al. argued that because Savolainen’s research “included many East Asian village dogs but few village dogs from other regions, their conclusion of high levels of East Asian diversity is likely a consequence of high levels of mitochondrial diversity in village dogs and not necessarily an indication of East Asian domestication.” Looking at mitochondrial DNA of African village dogs, Boyko et al. concluded that “local mtDNA diversity did not differ systematically between African regions and similarly sized regions in East Asia, the purported origin of domestic dogs.” They do not suggest Africa as a site of dog domestication, but do see their findings as putting Savolainen’s conclusions in doubt.

In 2013, Marie-Dominique Crapon de Caprona and Peter Savolainen published a paper, heavily laden with excellent photographs, to make the case for phenotype diversity among village dogs of southern China.  They summarize the prior arguments made by their school of thought on the locus of domestication issue:

“[T]he genetic diversity for [mtDNA and Y-chromosomal DNA] markers is distinctly higher for dogs in southern East Asia than in all other dog populations across the world.  Most noticeably, in the universal dog gene pool there are 10 principal genetic groups of mtDNA, and all these groups have been found in southern East Asia, while only subsets of this gene pool were found in other regions, for example, Europe (4 of 10 groups), Southwest Asia (5), and north China (5).  This gives a strong indication that today’s Domestic Dog (Canis familiaris) originated from wolves in southern Eastern Asia, thus suggesting a region not previously thought to be the place dog origins.” They argue that it “is unlikely that this richness of phenotypes would originate from a recent extensive crossbreeding to European dogs, the dogs … being traditionally bred in rural villages with no known influence of European breeds and therefore most probably indigenous to southern China.” 

Also in 2013, Niskanen et al., a team that included Savolainen, found that major histocompatibility complex (MHC) diversity was highest in Asian dogs, though Northeast Asia and Southwest Asia were nearly identical under this measure of diversity. They gave a number of scenarios that could explain their data, but preferred an estimate of around 500 individuals (translating into a census population of 1,200 to 1,500 individuals).  They see this large founding population as consistent with the argument of the Coppingers (2001), where taking advantage of food waste around villages “probably developed over a period of time and in an expanded region.”

Bottleneck 27,000 Years Ago

Lindblad-Toh and a massive number of colleagues (2005) concluded that linkage disequilibrium (LD) of single nucleotide polymorphisms (SNPs) were best explained as reflecting “two principal bottlenecks in dog history: early domestication and recent breed creation.”  The first bottleneck was estimated to be about 9,000 generations ago, or approximately 27,000 years ago. 

Starch Digestion

Most recently, Axelsson et al. (2013) argue that dog domestication was accompanied by selection at three genes with key roles in starch digestion. 

Rock Painting, Tassili n Ajjer, Algeria (Neolithic Agricultural Site)

“Our results show that adaptations that allowed the early ancestors of modern dogs to thrive on a diet rich in starch, relative to the carnivorous diet of wolves, constituted a crucial step in early dog domestication. This may suggest that a change of ecological niche could have been the driving force behind the domestication process, and that scavenging in waste dumps near the increasingly common human settlements during the dawn of the agricultural revolution may have constituted this new niche. In light of previous results describing the timing and location of dog domestication, our findings may suggest that the development of agriculture catalysed the domestication of dogs.”

This, of course, easily correlates with the argument that agriculture led to a final separation of dogs and wolves since dogs would now have to defend the livestock against wolves. 

Middle East Argument

In 2010, vonHoldt et al. concluded, based on a higher proportion of haplotype sharing of dogs with wolves from the Middle East, that wolves from that area “are a dominant source of genetic diversity for dogs rather than wolves from east Asia.” Although they find the Middle East to be the “primary source of genetic variation in the dog,” they accept that there could be “potential secondary sources of variation from Europe and east Asia.”   They note that the primary contribution of Middle Eastern wolves is consistent with the archeological record.

Wayne and vonHoldt (2012), in a paper summarizing some of their prior work, observe that “a large number of genes appear associated with the early phase of domestication” and that “much of the distinct morphologic diversity of dogs reflects variation in a relatively small number of genes.” (See also Boyko et al. 2010.)  Acknowledging that “the similarity of some specific East Asian ancient breeds and Chinese wolves suggests that wolves from this area contributed to the dog genome as well,” these two authors believe that “the significant component of haplotype sharing for 15-SNP windows implies both the Middle East and Europe may have contributed substantially to the genome of domestic dogs, a result that is consistent with the archeological record.” This indicates multiple domestication events and several locations. 

Southeast Asian Village Dogs

Brown et al. (2011) come closest to finding a common ground between the Middle Eastern and Asian origin theories.  They concluded “based on both matrilineal and patrilineal markers that extant dogs of Southeast Asia … harbor more genetic diversity than the Middle East.” They acknowledge that they did not test village dogs from “a large intervening portion of Asia….”  As to African breeds, they find haplotypes reflecting a “paternal lineage of dogs not present in Asia.”

They suggest a “deep divergence” of Middle Eastern and Southeast Asian village dog patrilines “reaching at least as far back as 10,000—16,000 years.”  Village dog populations of these two areas “must have originated either from a common gene pool thousands of years before present or from distinct groups of wolf or wolf-like founders, but are clearly not the product of post-Victorian expansion of dog breeds.”  The abstract indicates that this divergence predates the Neolithic ages. Current breeds identified as European and American “clustered in the Southeast Asia clade, which ran counter to expectations.”  Their “most parsimonious” explanation of this is, however, unsatisfactory:

“[T]he near complete lack of Middle Eastern haplotypes in Western breeds was unexpected given the relative proximity of Europe to the Middle East relative to East Asia. The most parsimonious interpretation of these findings would seem to be that modern European breed dogs are overwhelmingly derived from recently imported exotic stock and not reflective of ancient indigenous ancestry. This interpretation is also supported by findings in ancient DNA studies in Europe and the America’s, which have uniformly found discontinuities between ancient and modern dogs, indicating relatively recent replacements of historical dog populations with post-Victorian breed dogs.”

This would involve a wholesale replacement of a large number of breeds with no historical connection to the orient by Eastern breeds or types that have no phylogenetic similarity to European breeds (except arguably in village dogs, which were not generally carried anywhere).  It is much easier to imagine that European and Asian dogs have a common origin in Russia or Siberia, and that somehow these two groups separated after a separation of Middle Eastern dogs from the ancestors of both of them.  Brown et al., in discussing implications for future research, suggest expanded sampling in, among other areas, central and northern Eurasia.  Sampling these areas more extensively should be a priority for any research group involved in this debate. 

Middle Eastern Small Dogs

In 2010, Gray et al. concluded that “grey wolves of Middle East origin were slightly closer to domestic dogs” as to a specific size-relevant allele. Variants in the IGF1 (insulin-like growth factor 1) gene are “fixed in the majority of small distantly related dog breeds which suggests that small size evolved early in the history of domestication.” A few giant breeds (mastiffs, bullmastiffs, and rottweilers) share the “small” allele, but no wild canid so far tested has been found to have this variant.  They conclude that “in concordance with past archeological studies, our molecular analysis provides strong evidence for the early evolution of small size in dogs in the Middle East, more than 12,000 years ago.” As discussed in a prior blog, however, the conclusions of this group were immediately disputed. 

SYNTHESIZING ARCHEOLOGY AND GENETICS

A 2012 article by Greger Larson and a number of colleagues who have already been mentioned here, including Carles Vila and Kerstin Lindblad-Toh, noted the number of dog remains older than 12,000 years in many locations and older than 8,000 years everywhere within the maximal distribution of wolves, suggested that this implied “independent domestications of local populations of wolves, migration of humans possessing dogs, or the secondary acquisition of dogs by groups that were not involved in the domestication process.”  

The observation that dogs could be secondarily acquired by groups of humans that were not involved in the domestication process is important.  This must be part of the explanation for the almost complete disappearance of pre-Columbian dog types in the Americas after the arrival of European dogs.  (Castroviejo-Fisher et al. 2011)  Dingoes may well have arrived in Australia with seafaring peoples who did not stay, yet the dogs formed relationships with earlier inhabitants of the island (Smith and Litchfield 2009).  Indeed, the increasing importance of village dogs in research on the origins of dogs reflects a focus on dogs whose habitation and movements across areas are often not specifically connected with any human purpose.  It is not difficult to imagine that dogs in Eurasia would separate from a human encampment when a camp split, some of the dogs going with a new group, which may have included enemies of the original group. 

Very little is known about migration patterns in the Paleolithic.  Some parallels with human genetic similarities have allowed for speculation, however. Combined groups of people and dogs may have entered Tibet and Japan in the Holocene, or conceivably the late Paleolithic, as noted by Li and Zhang (2012):

“[I]ntriguingly, three [Tibetan Mastiff] haplotypes showed a genetic link between dogs of the Qing-Tibet Plateau and Japan…, similar to the genetic link between Tibetans and Japanese [peoples] …. Based on the rare derived haplotypes from the three major haplotypes in Tibet, it is prudent to conclude a Holocene origin for the Tibetans-Japanese linkage, while the hypothesis of Pleistocene migration towards both the Qing-Tibet Plateau and eastern seacoast to Japan needs more evidence.” 

It will be important to consider human migration data in relation to evidence for dog origins.  For instance, a recent study has argued for a human migration from Southeast Asia to East Asia during the Last Glacial Maximum (Cai et al. 2011), which may indicate that the somewhat different loci posited by Savolainen and his colleagues are the same as those posited by Brown and her colleagues.   

It should, in any case, not be imagined that domestication of wolves is easy.  As discussed in a prior blog, most geneticists have concluded that American wolves were not domesticated.  (This statement must be qualified, however, by reference to the fact that a degree of domestication occurred with certain South American canids, as discussed in another blog.)

CONCLUSION

Bison in Font-de-Gaume Cave (painting by Breuil, 1910)

Knowing full well that any pronouncements I have the hubris to make are likely to be made lies by future research, and accepting that my connections to science are now so attenuated as to not justify broadcast of my opinions in the first place, I will nevertheless stick my neck out.  I do believe that Germonpre has shifted the burden of proof, and that those who would argue that domestication is restricted to periods after the Last Glacial Maximum cannot ignore the evidence, both archeological and genetic, that there were significant changes to wolf-human relations beginning in the Aurignacian.  I also accept that those changes likely continued through the Last Glacial Maximum, though probably with significant bottlenecking (Brace et al. 2012), which reduced the variability found in partially domesticated wolves earlier. 

I am not convinced that there were multiple domestication events in the post-Last Glacial Maximum.  Earlier migrations could have led to separations within the original modified wolf population (or more likely populations, given the acknowledged diversity of the animals found at separate sites).  Such migrations could explain the divergence between Far Eastern and Middle Eastern dog groups, and a later separation, perhaps during the Last Glacial Maximum, could have occurred between Eurasian populations that went separately towards Asia and Europe.  It is hard to say how much refinement can be made to the Aurignacian argument without significantly more animals being identified as Upper Paleolithic dogs, and a full understanding would also require knowing considerably more about human migrations in the same period.

The following table collects the major dates and locations included in this discussion.

Years Before Present	Developments (genetic studies in red)	Locations	Sources
135,000-100,000	Early dating for dog domestication	Two clades closest to wolf sequences from eastern Europe	Vila et al. (1997)
41,000-38,500	Animal remains of early Upper Paleolithic Kostenki site include canids categorized as Pleistocene wolves; wolf bones found with other animal bones	River Don, Russia, near Voronezh	Germonpre et al. (2012)
38,000-30,000	Pierced objects, such as teeth, increasingly used as decoration; finds include at Grotte des Hyene at Brassempouy	Southwestern France	White (2003)
37,000-28,000	Aurignacian sites in southern Europe perhaps culturally distinct from northern Europe; bead types may indicate distinct language families.	Europe	Vandaeren and d’Errico
32,000 (cal. 36,000)	Large domestic dogs associated with Aurignacian culture (though other scholars, such as Pionnier-Capitain et al. question whether this may represent a divergent wolf population); the animals preyed primarily on horses and large bovids; researchers speculate dogs may have helped in tracking, hunting, or transport of large game, including mammoths.	Goyet cave in Samson Valley, Belgium	Germonpre et al. (2009)
29,950-27,850 (cal. 33,500-33,000)	Skull may represent an “incipient” dog in the early stages of domestication, but researchers argue that its lineage did not survive the Last Glacial Maximum (LGM).	Razboinichya Cave in Altai Mountains of southern Siberia	Ovodov et al. (2011)
30,000	Estimated divergence of wolves and dogs assuming continuing low level of gene flow between groups.	India (Middle East?)	Skoglund et al. (2010)
27,000	Early ancient genetic bottleneck eliminating much of early dog diversity.	East Asia (by secondary reference)	Lindblad-Toh et al. (2005)
27,000-26,000	Canids identified as Paleolithic dogs; Gravettian culture hunted mammoths, horse, bison, and reindeer; one dog or small wolf was found in a human burial zone; human occupation took place in warmer periods preceding LGM.	Piedmosti site, Czech Republic	Germonpre et al. (2012)
27,000-25,000	Gravettian site produced wolf vertebra with cut marks, possibly from dismembering or filleting the carcass.	Milovice Valley, Czech Republic	Svoboda et al. (2011)
26,500	Beginning of Last Glacial Maximum
26,000	Tracks of large dog or wolf and child in Chauvet cave; torch wipes made by this child were dated to c. 26,000 years before present; short length of medial fingers of canid were interpreted as being made by a large dog.	France	Germonpre et al. (2009)
21,000-20,000	Avdeevo Gravettian site included images of wolves; presence of large number of remains from foxes and wolves suggests inhabitants hunted for fur; perforated canines from foxes and wolves were used as adornment.	Russian Plain near Kursk	Gvozdover (1995): Germonpre et al. (2009 and 2012)
19,000	End of Last Glacial Maximum
17,000-13,000	Dog skulls similar in shape but slightly larger than Siberian huskies excavated in remains of dwelling of Epigravettian culture site; may have been cooperation in hunting but dogs were probably also eaten (holes in sides of skulls).	Eliseevichi Cave, Dnieper River basin, Russia	Sablin and Khlopachev; Germonpre et al. (2009)
17,000-11,000	Polychrome cave painting of wolf, Magdalenian culture	Font de Gaume cave, southwestern France	Capitan (1910)
16,300	Domestic Dog originated in southern China from several hundred wolves.	China, south of the Yangtze River	Pang et al. (2009)
16,000-10,000	Analysis of village dogs in both locations suggests Middle Eastern and Southeast Asian village dog partilines have “deep divergence.”	Broad sampling of village dogs in Southeast Asia	Brown et al. (2011)
15,000-11,500	Late Glacial small dogs found in southwest and northern France similar in size but distinguishable from dholes; cutmarks indicate dogs were sometimes eaten (“irregular and anecdotal in terms of subsistence strategy”); authors suggest “at least two different evolutionary scenarios for Late Glacial dogs’ domestication, and likely at least two independent areas for dog domestication.”	Pont d’Ambon, Montespan, Le Closeau, France	Pionnier-Capitan et al.
15,000-11,500	Medium-sized dogs associated with Natufian culture in Near East, including burials.	Israel	Davis and Valla (1978); Dayan (1994)
14,600-14,000	Domestic dog identified as Paleolithic.	Kesslerlock Cave, Switzerland	Napierala and Uerpmann, H.-P. (2010)
12,000	Possible simultaneous migration of dogs and men of same group into Tibet and Japan.	Human and canine migration out of China	Li and Zhang
10,500-9,700	Dog remains found in Hebei Province, NE China, as indicated by mandible dentition.	Nanzhuangtou	Yuan et al. (2008) (citing unpublished results)

Thanks to Richard Hawkins, Kingsbury Parker, Eric Krieger, and Brian Duggan for comments and improvements.  Thanks to Dr. Germonpre for clarifying dates. Thanks to Betty Murphy for assistance in finding sources at the library of the Heard Museum in Phoenix.  

Sources:

1. Axelsson, E., Ratnakumar, A., Arendt, M-J., Maqbool, K., Webster, M.T., Perloski, M., Liberg, O., Arnemo, J.M., Hedhammar, A., and Lindblad-Toh, K., (2013). The Genomic Structure of Dog Domestication Reveals Adaptation to a Starch-Rich Diet. Nature (published first online); doi:10.1038/nature11837.
2. Benecke, N., 1994. Archäozoologische Studien zur Entwicklung der Haustierhaltung.Akademie Verlag, Berlin.
3. Bleed, P. (2006). Living in the Human Niche. Evolutionary Anthropology, 15, 8-10.
4. Boyko, A.R., Boyko, R.H., Boyko, C.M., Parker, H.G., Castelhano, M., Corey, L., et al. (2009). Complex Population Structure in African Village Dogs and Its Implications for Inferring Dog Domestication History. PNAS, 106(33), 13903-13908.
5. Boyko, A.R., Quignon, P., Li, L., Schoenebeck, J.J., Degenhardt, J.D., Lohmueller, K.E., Zhao, K. et al. (2010). A Simple Genetic Architecture Underlies Morphological Variation in Dogs.  PlosONE, 8(8), e1000451. (In contrast to the results from association mapping of quantitative traits in humans and domesticated plants, we find that across dog breeds, a small number of quantitative trait loci (#3) explain the majority of phenotypic variation for most of the traits we studied. In addition, many genomic regions show signatures of recent selection, with most of the highly differentiated regions being associated with breed-defining traits such as body size, coat characteristics, and ear floppiness.”).
6. Brace, S., Palkopoulou, E., Dalen, L., Lister, A.M., Miller, R., Otte, M., Germonpre, M., Blockley, S.P.E., Stewart, J.R., and Barnes, I. (2012). Serial Population Extinctions in a Small Mammal Indicate Late Pleistocene Ecosystem Instability.  PNAS, 109(50), 20532-6 ("That we identify a series of population extinctions throughout the end-Pleistocene from a small-mammal species demonstrates an extensive and prolonged diversity loss and suggests a nonsize-biased reduction in ecological stability during the last glaciation, a pattern consistent with climatic and environmental change as key drivers for changes in Late Pleistocene biodiversity.")
7. Brown, S.K., Pedersen, N.C., Jafarishorijeh, S., Bannasch, D.L., Ahrens, K.D., Wu, J.-T., Okon, M., and Sacks, B.N. (2011). Phylogenetic Distinctiveness of Middle Eastern and Southeast Asian Village Dog Y Chromosomes Illuminate Dog Origins. PLoS ONE, 6(12), e28496.
8. Cai, Z., Qin, Z., Wen, B., Xu., S., Wang, Y., Lu, Y., Wei, L., Wang, C., Li, S., Huang, Z. Jin, L., Li, H., and the Genographic Consortium (2011).  Human Migration through Bottlenecks from Southeast Asia into East Asia during Last Glacial Maximum Revealed by Y Chromosomes.  PlosONE, 6(8), e24282.
9. Capitan, L., Breuil, H., and Peyrony, D. (1910). La Caverne de Font-de-Gaume aux Eyzies. Chene, Monaco.
10. Cartmill, M., and Smith, F.H. (2009). The Human Lineage.  Wiley-Blackwell, Hoboken.  (at 418, summarizing arguments of Joao Zilhao that the “Proto-Aurignacian commingles two different traditions of personal adornment—one (the use of modified marine shells) brought in from West Asia, and a second (the use of pierced and grooved teeth, bones, and fossils as beads) that has local antecendents in Europe.  The fossil evidence suggests that this second tradition as invented by Neandertals, before modern humans came on the scene.”).
11. Castroviejo-Fisher, S., Skoglund, P., Valadez, R., Vila, C., and Leonard, J.A. (2011). Vanishing Native American Dog Lineages. BMC Evolutionary Biology, 11, 73.
12. Clutton-Brock, J. (1977). Man-Made Dogs. Science, 197(4311), 1340-1342 ("It is because the social structure and hunting behavior of the wolf and man are so similar that their association is so closely bonded.")
13. Coppinger, Raymond, and Coppinger, Lorna (2001). Dogs: A Startling New Understanding of Canine Origin, Behavior & Evolution. New York, Scribner.
14. Coulson, D., and Campbell, A. (2001). Rock Art of the Tassili n Ajjer, Algeria.  In African Rock Art: Paintings and Engravings in Stone. Harry Abrams, New York.
15. Crapon de Caprona, M-D., and Savolainen, P. (2013). Extensive Phenotype Diversity among South Chinese Dogs. ISRN Evolutionary Biology, ID 62183.
16. Crockford, S.J., and Kuzmin, Y.V. (2012). Comments on Germonpré et al., Journal of Archaeological Science 36, 2009 “Fossil dogs and wolves from Palaeolithic sites in Belgium, the Ukraine and Russia: osteometry, ancient DNA and stable isotopes”, and Germonpré, Lázkičková-Galetová, and Sablin, Journal of Archaeological Science 39, 2012 “Palaeolithic dog skulls at the Gravettian Předmostí site, the Czech Republic”. Journal of Archaeological Science, 39(8), 2797-2801.
17. Davis, S.J.M., and Valla, F.R. (1978). Evidence for Domestication of the Dog 12,000 Years Ago in the Natufian of Israel. Nature, 276, 608-610.
18. Dayan, T. (1994). Early Domesticated Dogs of the Near East. Journal of Archaeological Science, 21, 633-640.
19. Derr, M. (2011). How the Dog Became the Dog. Overlook Press, New York.  (Generally accepting that Germonpre’s Paleolithic dogs were distinguishable from wolves: “Dogwolves were like second-generation immigrants in a community that clung to its old ways even while adapting to its new land.  Born near humans, they were more likely that the first-generation socialized wolves to seek to reproduce in or near their human settlement, and more of their offspring were become more consistently socialized to humans, more familiar to human society.”)
20. d’Errico, F. (2003). The Invisible Frontier. A Multiple Species Model for the Origin of Behavioral Modernity.  Evolutionary Anthropology, 12, 188-202.
21. Ding, Z-L., Oskarsson, M., Ardalan, A., Angleby, H., Dahlgren, L-G., Tepeli, C., Kirkness, E., Savolainen, P., and Zhang, Y-P. (2012)  Origins of Domestic Dog in Southern East Asia Is Supported by Analysis of Y-Chromosome DNA.  Heredity, 108, 507-514 (using one Tibetan mastiff as a Y DNA source).
22. Driscoll, C.A., and Macdonald, D.W. (2010). Top Dogs: Wolf Domestication and Wealth. Journal of Biology, 9(10). 
23. Eshleman, C. (2009). Lectures on the Ice-Age Painted Caves of Southwestern France.  Interval(le)s, 2.2-3.1, 235-270.
24. Garcia, M.A., 2005. Ichnologie ge´ne´ rale de la grotte Chauvet. Bulletin de la Societe Prehistorique Francaise, 102, 103–108.
25. Germonpre, M., Laznickova-Galetova, M., and Sablin, M. (2012). Paleolithic Dog Skulls at the Gravettian Piedmosti Site, the Czech Republic.  Journal of Archaeological Science, 39(1), 184-202.
26. Germonpre, M., Sablin, M.V., Stevens, R.E., Hedges, R.E.M., Hofreiter, M., Stiller, M., and Despres, V. (2009). Fossil Dogs and Wolves from Paleolithic Sites in Belgium, the Ukraine and Russia: Osteometry, Ancient DNA and Stable Isotopes. Journal of Archaeological Science, 36(2), 473-490.
27. Germonpre, M., Sablin, M.V., Stevens, Despres, V., Hofreiter, M., Laznickova-Galetova, M., Stevens, R.E., and Stiller, M. (2013). Paleolithic Dogs and the Early Domestication of the Wolf: A Reply to the Commons of Crockford and Kuzmin (2012) (2013). Journal of Archaeological Science, 40, 786-792.
28. Gray, M.M., Sutter, N.B., Ostrander, E.A., and Wayne, R.K. (2010). The IGF1 Small Dog Haplotype Is Derived From Middle Eastern Grey Wolves. BMC Biology, 8, 16.
29. Gvozdover, M. (1995). Art of the Mammoth Hunters: The Finds from Avdeevo. Oxbow Monograph 49. Oxbow Books Ltd., Oxford, UK.
30. Hoffecker, J.F., Kuz’mina, I.E., Syromyatnikova, E.V., Anikovich, M.V., Sinitsyn, A.A., Popov, V.V., and Holliday, V.T. (2010). Evidence for Kill-Butchery Events of Early Upper Paleolithic Age at Kostenki, Russia.  Journal of Archaeological Science 37, 1073-1089.
31. Holliday, V.T., Hoffecker, J.F., Goldberg, P., Macphail, R.I., Forman, S.L., Anikovich, M., and Sinitsyn, A. (2007). Geoarchaeology of the Kostenki-Borshchevo Sites, Don River Valley, Russia.  Geoarchaeology, 22(2), 181-22.
32. Ho, S.Y.W., Phillips, M.J., Cooper, A., and Drummond, A.J. (2005). Time Dependency of Molecular Rate Estimates and Systematic Overestimation of Recent Divergence Times.  Molecular Biology and Evolution, 22(7), 1561-8.
33. Klutsch, C., and Savolainen, P. (2011). Geographical Origin of the Domestic Dog. Encyclopedia of Life Sciences. John Wiley and Sons, New York.
34. Kuzmin, Y.V. (2007). Chronological Framework of the Siberian Paleolithic: Recent Achievements and Future Directions. Radiocarbon, 49, 757-766.
35. Larson, G., Karlsson, E.K., Perri, A., Webster, M.T., Ho, S.Y.W., Peters, J., Stahl, P.W., Piper, P.J., Lingaas, F., Fredholm, M., Comstock, K.E., Modiano, J.F., Schelling, C., Agoulnik, A.I., Leegwater, P.A., Dobney, K., Vigne, J.-D., Vila, C., Andersson, L., and Lindblad-Toh, K. (2012). Rethinking Dog Domestication by Integrating Genetics, Archeology, and Biogeography. Proceedings of the National Academy of Sciences, 109(23), 8878-83.
36. Li, Q., Liu, Z., Li, X., Zhao, X., Dong, L., Pan, Z., Sun, Y., Li, N., Xu, Y., and Xie, Z. (2008). Origin and Phyologenetic Analysis of Tibetan Mastiff Based on the Mitochondrial DNA Sequence. Journal of Genetics and Genomics, 35, 335-340.
37. Li, Y. and Zhang, Y-P. (2012).  High Genetic Diversity of Tibetan Mastiffs Revealed by mtDNA Sequences.  Chinese Science Bulletin, 57(13), 1483-1487. doi: 10.1007/s11434-012-4995-4.
38. Lindblad-Toh, K., Wade, C.M., Mikkelsen, T.S., Karlsson, E.K., Jaffe, D.B., Kamal, M., et al. (2005). Genome Sequence, Comparative Analysis and Haplotype Structure of the Domestic Dog. Nature, 438(8), 803-819.
39. Losey, R.J., Bazaliiskii, V.I., Garvie-Lok, S., Germonpre, M., Leonard, J.A., Allen, A.L., Katzenberg, M.A., and Sablin, M.V. (2011). Canids as Persons: Early Neolithic Dog and Wolf Burials, Cis-Baikcal, Siberia.  Journal of Anthropological Archaeology, 30, 174-189.
40. Morey, D.F. (2010). Dogs: Domestication and the Development of a Social Bond.  Cambridge University Press, New York.
41. Napierala, H., and Uerpmann, H.-P. (2010). A “New” Palaeolithic Dog from Central Europe.  International Journal of Osteoarchaeology, 22(2), 127-137.
42. Niskanen, N.K., Hagstrom, E., Lohi, H., Ruokonen, M., Esparza-Salas, R., Aspi, J., and Savolainen, P. (2013). MHC Variability Supports Dog Domestication from a Large Number of Wolves: High Diversity in Asia.  Heredity, 110, 80-85.
43. Pang, J-F., Kluetsch, C., Zou, X-J., Ahang, A., Luo, Li-Y., Agleby, H., Ardalan, A., Ekstrom, C., Skollermos, A., Lundeberg, J., Matsumura, S., Leitner, T., Zhang, Y-P., and Savolainen, P. (2009). mtDNA Data Indicates a Single Origin for Dogs South of Yangtze River, Less Than 16,300 Years Ago, from Numerous Wolves. Molecular Biology and Evolution, 26(12), 2849-64.
44. Pionnier-Capitan, M., Bemilli, C., Bodu, P., Celerier, G., Ferrie, J.-G.,Fosse, P., Garcia, M., and Vigne, J.-D. (September 2011). New Evidence for Upper Palaeolithic Small Domestic Dogs in South-Western Europe. Journal of Archaeological Science, 38(9), 2123-2140.
45. Riel-Salvatore, J. (2010). A Niche Construction Perspective on the Middle-Upper Paleolithic Transition in Italy.  Journal of Archaeological Method and Theory, 17(4), 323-355.
46. Roebroeks, W. (2008). Time for the Middle to Upper Paleolithic Transition in Europe. Journal of Human Evolution, 55, 918-926.
47. Sablin, M.V. and Khlopachev, G.A. (2002). The Earliest Ice Age dogs: Evidence from Eliseevichi 1. Current Anthropology, 43, 795e799.
48. Savolainen, P., Shang, Y-P., L. Luo, Lundeberg, L. and Leitner, T. (2002). Genetic Evidence for an East Asian Origin of Domestic Dogs. Science, 298, 1610-1613.
49. Schleidt, W.M., and Shalter, M.D.  (2003). Co-Evolution of Humans and Canids, An Alternative View of Dog Domestication: Homo Homini Lupus?  Evolution and Cognition, 9(1), 57-72.
50. Sharma, D.K., Maldonado, J.E., Jhala, Y.V., and Fleischer, R.C. (2003). Ancient Wolf Lineages in India. Proceedings of the Royal Society of London B (Suppl.). doi 10.1098/rsbl.2003.0071 (finding: “the Indian subcontinent has three divergent, ancient and apparently parapatric mtDNA lineages within the morphologically delineated wolf.  No haplotypes of either novel lineage are found within a sample of 37 Indian (or other) dogs.  Thus, we find no evidence that these two taxa played a part in the domestication of canids”).
51. Skoglund, P., Gotherstrom, A., and Jakobsson, M. (2010).  Estimation of Population Divergence Times from Non-Overlapping Genomic Sequences: Examples from Dogs and Wolves.  Molecular Biology and Evolution, 28(4), 1505-1517.
52. Smith, B.P. and Litchfield, C.A. (2009) A Review of the Relationship between Indigenous Australians, Dingoes (Canis dingo) and Domestic Dogs (Canis familiaris), Anthrozoos, 22(2), 111-128.
53. Svoboda, J., Bochenski, Z.M., Culikova, V., Dohnalova, A., Hladilova, S., Hlozek, M. et al. (2011) Paleolithic Hunting in a Southern Moravian Landscape: The Case of Milovice IV, Czech Republic. Geoarchaeology, 26(6), 838-866.
54. Vanhaeren, M., and d’Errico, F. (2006). Aurignacian Ethno-Linquistic Geography of Europe Revealed by Personal Ornaments.  Journal of Archaeological Science, 33(8), 1105-1128.
55. Verginelli, F., Capelli, C., Valentina, C., Muisani, M., Falchetti, M., Ottini, L., Palmirotta, R., Tagliacozzo, A., Mazzorin, I.D.G, and Mariani-Costantini, R. ( 2005). Mitochondrial DNA from Prehistoric Canids Highlights Relationships Between Dogs and South-East European Wolves. Molecular Biology and Evolution, 22(12), 2541-2551.
56. Vila, C., Savolainen, P., Maldonado, J.E., Amorim, I.R., Rice, J.E., Honeycutt, R.L., Crandall, K.A., Lundeberg, J., and Wayne, R.K. (1997). Multiple and Ancient Origins of the Domestic Dog.  Science, 276, 1687-9.
57. Vila, C., Seddon, J., and Ellegren (2005). Genes of Domestic Mammals Augmented by Backcrossing with Wild Ancestors.  Trends in Genetics, 21(4), 214-218.
58. vonHoldt, B.M., Pollinger, J.P., Lohmueller, K.E., et al. (2010).  Genome-Wide SNP and Haplotype Analyses Reveal a Rich History Underlying Dog Domestication.  Nature, 464(8 April 2010) doi:10.1038/nature08837.
59. Wayne, R.K., and vonHoldt, B.M. (2012). Mammalian Genome, 23, 3-18.
60. White, R. (2003). Systems of Personal Ornamentation in the Early Upper Paleolithic: Methodological Challenges and New Observations. In Mellars, P., Boyle, K., Bar-Yosef, O., Stringer, C. (Eds.), Rethinking the Human Revolution: New Behavioural and Biological Perspectives on the Origin and Dispersal of Modern Humans. McDonald Institute Monographs.
61. Ye, J-H., Ren, D-R., Xie, A-F., Wu, X-P., Xu, L., Fu, P-F., Zhao, H-A., and Yang, Q-Y. (2009). Microsatellite-Based Genetic Diversity and Evolutionary Relationships of Six Dog Breeds.  Asian-Australian Journal of Animal Science, 22(8), 1102-1106.
62. Yuan, J., Jian-Lin, H., and Blench, R. (2008). Livestock in Ancient China. Chapter in Past Human Migrations in East Asia: Matching Archaeology, Linguistics and Genetics (Sanchez-Maza, Blench, Ross, Peiros, and Lin, eds.) Routledge, New York, NY.
63. Zhao, M., Kong, Q-P., Wang, H-W., Peng, M-S., Xie, X-D., Wang, W-Z., Jiayang, Duan, J-G., Cai, M-C., Zhao, S-N., Cidanpingcuo, Tu, Y-Q., Wu, S-F., Yao, Y-G., Bandelt, H-J., and Zhang, Y-P. (2009). Mitochondrial Genome Evidence Reveals Late Paleolithic Settlement on the Tibetan Plateau.  PNAS, 106(5), 21230-21235.