Origin of the domestic dog

The dog diverged from a now-extinct population of wolves immediately before the Last Glacial Maximum, when much of Eurasia was a cold, dry mammoth steppe biome.

The origin of the domestic dog is not clear. The domestic dog is a member of genus Canis (canines) that forms part of the wolf-like canids, and is the most widely abundant carnivore.^[1][2][3] The closest living relative of the dog is the gray wolf and there is no evidence of any other canine contributing to its genetic lineage.^[1][2][4][5] The dog and the extant gray wolf form two sister clades,^[5][6][7] with modern wolves not closely related to the wolves that were first domesticated.^[6][7] The archaeological record shows the first undisputed dog remains buried beside humans 14,700 years ago,^[8] with disputed remains occurring 36,000 years ago.^[9] These dates imply that the earliest dogs arose in the time of human hunter-gatherers and not agriculturists.^[2][6] The dog was the first domesticated species.^{[7][10][11][12]}

Where the genetic divergence of dog and wolf took place remains controversial, with the most plausible proposals spanning Western Europe,^[13][2] Central Asia,^[13][14] and East Asia.^[13][15] This has been made more complicated by the most recent proposal that fits the available evidence, which is that an initial wolf population split into East and West Eurasian wolves, these were then domesticated independently before going extinct into two distinct dog populations between 14,000–6,400 years ago, and then the Western Eurasian dog population was partially and gradually replaced by East Asian dogs that were brought by humans at least 6,400 years ago.^[13][16][17]

Canid and human evolution

Six million years ago at the close of the Miocene era, the earth's climate was gradually cooling and this would lead to the glaciations of the Pliocene and the Pleistocene (the Ice Age). In many areas the forests and savannahs were being replaced with steppe or grasslands and only those creatures that could adapt would survive. On opposite sides of the planet, two very different lineages would adapt to these changes and their evolution would produce two species that would become the most widely distributed of mammals. In southern North America, small woodland foxes were growing bigger and becoming more adapted to running, and by the late Miocene the first of the genus Canis had arisen, the ancestors of coyotes, wolves and the domestic dog. In eastern Africa, a split was occurring among the large primates. Some would remain in the trees, while others would move out of the trees, learn to walk upright, develop enlarged brains, and learn to avoid predators while becoming a predator themselves in the more open country.^[18] The two lineages would ultimately meet on the Eurasian continent. "They were individual animals and people involved, from our perspective, in a biological and cultural process that involved linking not only their lives but the evolutionary fate of their heirs in ways, we must assume, they could never have imagined."^[19]

Further Information: Canid evolution

Dog evolution

Dog evolution (from the Latin evolutio: "unrolling")^[20] is the biological descent with modification^[21] that led to the domestic dog. This process encompasses small-scale evolution (changes in gene frequency in a population from one generation to the next) and large-scale evolution (the descent of different species from a common ancestor over many generations).^[22]

Genetics, archaeology and morphology

Gray wolf divergence

wolf/dog ancestor New World clade Mexico North America Old World clade Dog Old World wolves Asian highland Asian lowland Middle East Europe

Whole-genome phylogenetic tree - extant gray wolf populations[1]

The domestic dog is the most widely abundant large carnivore.^[2][1][3] When and where dogs were first domesticated has vexed geneticists for the past 20 years and archaeologists for many decades longer.^[7] Identifying the earliest dogs is difficult because the key morphological characters that are used by zooarchaeologists to differentiate domestic dogs from their wild wolf ancestors (size and position of teeth, dental pathologies, and size and proportion of cranial and postcranial elements) were not yet fixed during the initial phases of the domestication process. The range of natural variation among these characters that may have existed in ancient wolf populations, and the time it took for these traits to appear in dogs, are unknown.^[10]

However, recent studies based on genetics propose four generalizations about dogs.^[23]

• Over the past million years, numerous wolf-like forms existed but their turnover has been high, and modern wolves are not the lineal ancestors of dogs.^{[2][6][1][24]} Although research had suggested that dogs and wolves were genetically very close relatives,^[5][25][26] later phylogenetic analysis strongly supported the hypothesis that the dog forms a monophyletic clade that is sister to Eurasian wolves, and these together form a sister clade to North American wolves.^[1][23] This indicates that an extant wolf population that is the ancestor to dogs has not been found and is presumed extinct.^[6][7] The dog is not a separate species to the wolf.^[1][23]

• The dog was the first domesticated species^{[7][10][11][12]} and appeared more than 15,000 years before present (YBP), with recent studies proposing a divergence time closer to 27,000 YBP.^{[1][16][27][6][2]} The dog was established across Eurasia before the end of the Late Pleistocene era, well before cultivation and the domestication of other animals around 10,000 YBP,^[10] indicating that dogs were domesticated by hunter-gatherers and not early agriculturalists. Studies support two population bottlenecks had occurred to the dog lineage, one due to the initial domestication and one due to the formation of dog breeds.^[23]

• Dogs show both ancient and modern lineages. The ancient lineages appear most in Asia but least in Europe because the Victorian era development of modern dog breeds used little of the ancient lineages.^[16][14][4] All dog populations (breed, village, and feral) show some evidence of genetic admixture between modern and ancient dogs. Some ancient dog populations that once occupied Europe and the New World no longer exist.^{[16][7][2][28]} This implies that some ancient dog populations were entirely replaced and others admixed over a long period of time.^[23]

• There was admixture between dog and regional wolf populations except on the Tibetan Plateau and in the New World wolves.^[1][6] This admixture has occurred throughout history and as dogs expanded across the landscape. There are some dog populations that show recent admixture with wolves.^[1][23]

The extinction of the wolves that were the direct ancestors of dogs, and the sustained admixture between different dog and wolf populations over at least the last 10,000 years, has blurred the genetic signatures and confounded efforts of researchers at pinpointing the origins of dogs.^[7][10]

Time of divergence

Paleoecology

Mammoth bone dwelling, Mezhirich site, Ukraine

During the last Ice Age, the most recent peak is known as the Last Glacial Maximum when a vast mammoth steppe stretched from Spain eastwards across Eurasia and over the Bering land bridge into Alaska and the Yukon. The continent of Europe was much colder and drier than it is today, with polar desert in the north and the remainder steppe or tundra. Forest and woodland were almost non-existent except for isolated pockets in the mountain ranges of southern Europe.^[29] The Late Pleistocene was characterized by a series of severe and rapid climate oscillations with regional temperature changes of up to 16 °C, which has been correlated with Pleistocene megafaunal extinctions. There is no evidence of megafaunal extinctions at the height of the Last Glacial Maximum, indicating that increasing cold and glaciation were not factors. Multiple events appear to have caused the rapid replacement of one species by one within the same genus, or one population by another within the same species, across a broad area. As some species became extinct, so too did the predators that depended on them.^[30] The ancestors of modern humans first reached Europe with their remains dated 43,000-45,000 years BP in Italy^[31] and in Britain.^[32]

See further: Paleoecology at this time

Probable ancestor

During the Last Glacial Maximum there were two types of wolf. The cold north of the Holarctic was spanned by a large, robust, wolf ecomorph that specialised in preying on megafauna. Another more slender form lived in the warmer south in refuges from the glaciation. When the planet warmed and the Late Glacial Maximum came to a close, whole species of megafauna became extinct along with their predators, leaving the more gracile wolf to dominate the Holarctic. The more gracile wolf was the ancestor of the modern gray wolf, which is the dog's sister but not its ancestor as the dog shows a closer genetic relationship to the now-extinct megafaunal wolf.

See further: Two wolf haplogroups

Evolutionary divergence

DNA evidence indicates that the dog, the modern gray wolf (above) and the now-extinct Taimyr wolf diverged from a now extinct wolf that once lived in Europe.

The date estimated for the evolutionary divergence of a domestic lineage from a wild one does not necessarily indicate the start of the domestication process but it does provide an upper boundary. The divergence of the domestic horse from the lineage that lead to the modern Przewalski’s horse is estimated at 45,000 YBP but the archaeological record indicates 5,500 YBP. The variance could be due to the modern wild population not being the direct ancestor of the domestic one, or the impact of a split due to climate, topography, or other environmental changes. The divergence time does not imply domestication during this specific period.^[13] Earlier researchers had proposed that the "dog was the dog before it was domesticated",^[33] and that the ancestor of Canis familiaris was a wild Canis familiaris.^[34]

Early mitochondrial DNA analysis indicated that if the dog had descended from the modern gray wolf then the divergence would have occurred 135,000 YBP.^[5] Two later studies using whole genome sequencing indicated divergence times of 32,000 YBP^[35] or 11,000-16,000 YBP,^[6] with the assumed mutation rate "the dominant source of uncertainty in dating the origin of dogs."^[6]

See further: Mutation rate timing issue

In 2015, a study was conducted on a partial rib-bone (designated as Taimyr-1) found near the Bolshaya Balakhnaya River in the Taymyr Peninsula, Arctic North Asia, that was AMS radiocarbon dated to 34,900 YBP. The sample provided the first draft genome from the cell nucleus of a Pleistocene carnivore and the sequence was identified as belonging to Canis lupus.^[27] The sequence indicated that the Taimyr-1 lineage was separate to modern wolves and dogs. Using the Taimyr-1 specimen's radiocarbon date in addition to its genome sequence compared to that of a modern wolf, a direct estimate of the mutation rate in dogs and wolves could be made to calculate the time of divergence. The study indicated that the Taimyr-1 population, gray wolves and dogs diverged from a now-extinct common ancestor before the peak of the Last Glacial Maximum 27,000-40,000 years ago. Such an early divergence is consistent with several paleontological reports of dog-like canids dated up to 36,000 YBP, as well as evidence that domesticated dogs most likely accompanied early colonizers into the Americas.^[27]

The study proposed that the timing of this separation of the dog and wolf did not have to coincide with selective breeding by humans.^{[27]:page3[36][13]}

Place of divergence

Where the genetic divergence of dog and wolf took place remains controversial, with the most plausible proposals spanning Western Europe,^[13][2] Central Asia,^[13][14] and East Asia.^[13][15] This has been made more complicated by the most recent proposal that fits the available evidence, which is that an initial wolf population split into East and West Eurasian wolves, these were then domesticated independently before going extinct into two distinct dog populations between 14,000-6,400 years ago, and then the Western Eurasian dog population was partially and gradually replaced by East Asian dogs that were brought by humans at least 6,400 years ago.^[13][16][17]

Using modern DNA

South East Asia: In 2009, a study of the maternal mitochondrial genome placed the origin in south-eastern Asia south of the Yangtze River as more dog haplogroups had been found there.^[37] Paternal Y-chromosome DNA sequences indicated the south-western part of south-eastern Asia that is south of the Yangtze River (comprising South-East Asia and the Chinese provinces of Yunnan and Guangxi) because of the greater diversity of yDNA haplogroups found in that region.^[38] A criticism of this proposal is that no wolf remains have been found in this region and the earliest archaeological evidence of a dog dates to only 4,700 YBP.^[10]

Middle East: In 2010, a study using single nucleotide polymorphisms indicated that dogs originated in the Middle East due to the greater sharing of haplotypes between dogs and Middle Eastern gray wolves, else there may have been significant admixture between some regional breeds and regional wolves.^[4] In 2011, a study found that there had been dog-wolf hybridization and not an independent domestication.^[6][39]

East Asia: In 2002, a study of maternal mDNA found that the dog diverged from its ancestor in East Asia because there were more dog mDNA haplotypes found there than in other parts of the world,^[40] but this was rebutted because village dogs in Africa also show a similar haplotype diversity.^[41] In 2015, a whole genome analysis of modern dog and wolf sequences concluded that based on the genetic diversity of today's East Asian dogs, the dog had originated in southern East Asia, followed by a migration of a subset of ancestral dogs 15,000 YBP towards the Middle East, Africa and Europe and reaching Europe 10,000 YBP. Then, one of these lineages migrated back to northern China and admixed with endemic Asian lineages before migrating to the Americas.^[15] A criticism of this proposal is that no dog remains date beyond 12,000 YBP in this region but date to 14,000 YBP in western Europe, however it is accepted that archaeological studies in the Far East are generally lagging behind those in Europe.^[10]

Central Asia: In 2015, a study looked at 85,805 genetic markers of autosomal, maternal mitochondrial genome and paternal Y chromosome diversity in 4,676 purebred dogs from 161 breeds and 549 village dogs from 38 countries. Some dog populations in the Neotropics and the South Pacific are almost completely derived from European stock, and other regions show clear admixture between indigenous and European dogs. The indigenous dog populations of Vietnam, India, and Egypt show minimal evidence of European admixture, and exhibit indicators consistent with a Central Asian domestication origin, followed by a population expansion in East Asia. The study could not rule out the possibility that dogs were domesticated elsewhere and subsequently arrived in and diversified from Central Asia. Studies of extant dogs cannot exclude the possibility of earlier domestication events that subsequently died out or were overwhelmed by more modern populations.^[14]

No agreement using modern DNA: In 2016, a whole-genome study of wolves and dogs concluded that admixture had confounded the ability to make inferences about the place of dog domestication. Past studies based on single-nucleotide polymorphisms,^[4] genome-wide similarities with Chinese wolves,^[15] and lower linkage disequilibrium^[14] might reflect regional admixture between dogs with wolves and gene flow between dog populations, with divergent dog breeds possibly maintaining more wolf ancestry in their genome. The study proposed that the analysis of ancient DNA might be a better approach.^[1]

Using ancient DNA

The 14,500-year-old upper-right jaw of a Pleistocene wolf found in Kesslerloch Cave, Switzerland, is the sister to 2/3 of modern dogs^[2] (courtesy Hannes Napierala)

In 1868, Charles Darwin wrote that some authors at the time proposed an unknown or extinct species was the ancestor of the dog.^[42] In 1934, an eminent paleontologist indicated that the ancestor of the dog lineage may have been the extinct Canis lupus variabilis.^[43] In 1999, a study emphasized that while molecular genetic data seem to support the origin of dogs from wolves, dogs may have descended from a now extinct species of canid whose closest living relative was the wolf.^[25] The dog's lineage may have been contributed to from a ghost population. The advent of rapid and inexpensive DNA sequencing technology has made it possible to significantly increase the resolving power of genetic data taken from both modern and ancient domestic dog genomes. Attention was now turned to studies based on ancient DNA from fossil canids.^[10]

Europe: In 2013, a study analysed the complete and partial mitochondrial genome sequences of 18 fossil canids dated from 1,000 to 36,000 YBP from the Old and New Worlds, and compared these with the complete mitochondrial genome sequences from modern wolves and dogs. Phylogenetic analysis showed that modern dog mDNA haplotypes resolve into four monophyletic clades with strong statistical support, and these have been designated by researchers as clades A-D.^[2][5][44] Based on the specimens used in this study, clade A included 64% of the dogs sampled and these were sister to a 14,500 YBP wolf sequence from the Kesserloch cave in Switzerland, with a most recent common ancestor estimated to 32,100 YBP. This group of dogs matched three fossil pre-Columbian New World dogs dated between 1,000 and 8,500 YBP, which supported the hypothesis that pre-Columbian dogs in the New World share ancestry with modern dogs and that they likely arrived with the first humans to the New World. Clade B included 22% of the dog sequences and was related to modern wolves from Sweden and the Ukraine, with a common recent ancestor estimated to 9,200 YBP. However, this relationship might represent mitochondrial genome introgression from wolves because dogs were domesticated by this time. Clade C included 12% of the dogs sampled and these were sister to two ancient dogs from the Bonn-Oberkassel cave (14,700 YBP) and the Kartstein cave (12,500 YBP) near Mechernich in Germany, with a common recent ancestor estimated to 16,000-24,000 YBP. Clade D contained sequences from 2 Scandinavian breeds (Jamthund, Norwegian Elkhound) and were sister to an ancient wolf-like canid from Switzerland, with a common recent ancestor estimated to 18,300 YBP. Its branch is phylogenetically rooted in the same sequence as the "Altai dog" (not a direct ancestor). The data from this study indicated a European origin for dogs that was estimated at 18,800–32,100 years ago based on the genetic relationship of 78% of the sampled dogs with ancient canid specimens found in Europe.^[2] The data supports the hypothesis that dog domestication preceded the emergence of agriculture^[5] and was initiated close to the Last Glacial Maximum when hunter-gatherers preyed on megafauna.^[2]

The study found that three ancient Belgium canids (the 36,000 YBP "Goyet dog" cataloged as Canis species, along with Belgium 30,000 YBP and 26,000 years YBP cataloged as Canis lupus) formed an ancient clade that was the most divergent group. The study found that the skulls of the "Goyet dog" and the "Altai dog" had some dog-like characteristics and proposed that the may have represented an aborted domestication episode. If so, there may have been originally more than one ancient domestication event for dogs^[2] as there was for domestic pigs.^[45]

A criticism of the European proposal is that dogs in East Asia show more genetic diversity. However, dramatic differences in genetic diversity can be influenced both by an ancient and recent history of inbreeding.^[15] A counter-comment is that the modern European breeds only emerged in the 19th Century, and that throughout history global dog populations experienced numerous episodes of diversification and homogenization, with each round further reducing the power of genetic data derived from modern breeds to help infer their early history.^[10]

Arctic North-East Siberia: In 2015, a study looked at the mitochondrial control region sequences of 13 ancient canid remains and one modern wolf from five sites across Arctic north-east Siberia. The fourteen canids revealed nine mitochondrial haplotypes, three of which were on record and the others not reported before. The phylogentic tree generated from the sequences showed that four of the Siberian canids dated 28,000 YBP and one Canis c.f. variabilis dated 360,000 YBP were highly divergent. The haplotype designated as S805 (28,000 YBP) from the Yana River was one mutation away from another haplotype S902 (8,000 YBP) that represents Clade A of the modern wolf and domestic dog lineages. Closely related to this haplotype was one that was found in the recently-extinct Japanese wolf. Several ancient haplotypes were oriented around S805, including Canis c.f. variabilis (360,000 YBP), Belgium (36,000 YBP - the "Goyet dog"), Belgium (30,000 YBP), and Konsteki, Russia (22,000 YBP). Given the position of the S805 haplotype on the phylogenetic tree, it may potentially represent a direct link from the progenitor (including Canis c.f. variabilis) to the domestic dog and modern wolf lineages. The gray wolf is thought to be ancestral to the domestic dog, however its relationship to C. variabilis, and the genetic contribution of C. variabilis to the dog, is the subject of debate.^[46]

The Zhokhov Island (8,700 YBP) and Aachim (1,700 YBP) canid haplotypes fell within the domestic dog clade, cluster with S805, and also share their haplotypes with - or are one mutation away from - the Tibetan wolf (C. l. chanco) and the recently-extinct Japanese wolf (C. l. hodophilax). This may indicate that these canids retained the genetic signature of admixture with regional wolf populations. Another haplotype designated as S504 (47,000 YBP) from Duvanny Yar appeared on the phylogenetic tree as not being connected to wolves (both ancient and modern) yet ancestral to dogs, and may represent a genetic source for regional dogs.^[46]

Eight thousand years ago, the arctic Zhokhov people made sophisticated sleds and bred sled dogs. Dog remains indicate draught dogs close to present-day Siberian Huskies in looks and weight. Their weight is the key factor in determining thermo-regulation, hardiness and working ability, with their weight staying in the 23-27 kg bracket and not exceeding 27 kg. They also possessed large hounds, probably for bear hunting.^[47]

See further: Hybrid speciation and Introgression

Archaeological evidence

Domesticated dogs are more clearly identified when they are associated with human occupation, and those interred side-by-side with human remains provide the most conclusive evidence,^[48] (refer to the table below - 14,708 YBP Bonn-Oberkassel dog).

The table below lists proposed early dog specimens, their location, and timing in years before present (listing the earliest estimate from the earliest and latest estimates provided) and color-coded as purple - Western Eurasia, red - Eastern Eurasia and green - Central Eurasia. The archaeological evidence shows the first dog remains to have been found early in both Western Eurasia and Eastern Eurasia, but not between them in Central Asia until much later.^[16]

Years BP	Location	Finding
36,000–14,708	Europe	Numerous disputed specimens across time that are proposed to be either Paleolithic dogs[9] or wolves that are morphologically and genetically distinct from modern wolves.[13]
14,708	Bonn-Oberkassel, Germany	Undisputed dog mandible directly associated with a human double grave of a 50-year-old man and a 20-25-year-old woman dated 14,708-13,874.[49] In 2013, the DNA sequence was identified as Canis lupus familiaris - dog.[2] Mitochondrial DNA analysis confirms that the Oberkasseler animal skeleton is a direct ancestor of today’s dogs.[8]
13,000	Palegawra, Iraq	Mandible[50]
12,900	Ushki I, Kamchatka, Russia	Complete skeleton[51]
12,790	Nanzhuangtou, China	31 fragments including a complete mandible[52]
12,500	Kartstein cave, Mechernich, Germany	Ancient dog skull. In 2013, the DNA sequence was identified as Canis lupus familiaris i.e. dog.[2]
12,450	Yakutia, Siberia	Mummified carcass. The "Black Dog of Tumat" was found frozen into the ice core of an oxbow lake steep ravine at the middle course of the Syalaah River in the Ust-Yana region. DNA analysis confirmed it as an early dog.[53]
12,000	Ain Mallaha (Eynan) and HaYonim terrace, Israel	Three canid finds. A diminutive carnassial and a mandible, and a wolf or dog puppy skeleton buried with a human during the Natufian culture.[54]
9,000	Jiahu site, China	Eleven dog interments. Jaihu is a Neolithic site 22 kilometers north of Wuyang in Henan Province.[55]
8,000	Svaerdborg site, Denmark	Three different dog types recorded at this Maglemosian culture site.[56]
7,425	Baikal region, Russia, Central Asia	Dog buried in a human burial ground. Additionally, a human skull was found buried between the legs of a "tundra wolf" dated 8,320 BP (but it does not match any known wolf DNA). The evidence indicates that as soon as formal cemeteries developed in Baikal, some canids began to receive mortuary treatments that closely paralleled those of humans. One dog was found buried with four red deer canine pendants around its neck dated 5,770 BP. Many burials of dogs continued in this region with the latest finding at 3,760 BP, and they were buried lying on their right side and facing towards the east as did their humans. Some were buried with artifacts, e.g., stone blades, birch bark and antler bone.[57]

Newgrange dog – two domestication events

In 2009, a study looked at the two earliest dog skulls that had been found at Eliseevich 1 in comparison to other much earlier but morphologically similar fossil skulls that had been found across Europe and concluded that the earlier specimens were "Paleolithic dogs", which were morphologically and genetically distinct from Pleistocene wolves that lived in Europe at that time. These also include the 36,000-year-old "Goyet dog" and the 33,000-year-old "Altai dog".^[9]

Later studies suggested that it was possible for multiple primitive forms of the dog to have existed, including in Europe.^[15] European dog populations had undergone extensive turnover during the last 15,000 years that has erased the genomic signature of early European dogs,^[14][58] the genetic heritage of the modern breeds has become blurred due to admixture,^[10] and there was the possibility of past domestication events that had gone extinct or had been largely replaced by more modern dog populations.^[14]

In 2016, a study compared the mitochondrial DNA and whole-genome sequences of a world-wide panel of modern dogs, the mDNA sequences of 59 ancient European dog specimens dated 14,000-3,000 YBP, and the nuclear genome sequence of a dog specimen that was found in the Late Neolithic passage grave at Newgrange, Ireland and radiocarbon dated at 4,800 YBP. A genetic analysis of the Newgrange dog showed that it was male, did not possess genetic variants associated with modern coat length nor color, was unable to process starch as efficiently as modern dogs but more efficiently than wolves, and showed ancestry from a population of wolves that could not be found in other dogs nor wolves today.^[16] As the taxonomic classification of the "proto-dog" Paleolithic dogs as being either dogs or wolves remains controversial, they were excluded from the study.^[16]:Sup The phylogenetic tree generated from mDNA sequences found a deep division between the Sarloos wolfdog and all other dogs, indicating that breed's recent deriving from the German Shepherd and captive gray wolves. The next largest division was between Eastern Asian dogs and Western Eurasian (Europe and the Middle East) dogs that had occurred between 14,000-6,400 YBP, with the Newgrange dog clustering with the Western Eurasian dogs. The northern breed Greenland dog and the Siberian husky were poorly supported in the tree, possibly indicating mixed ancestry.^[45] (See also Taimyr wolf admixture)

The Newgrange and ancient European dog mDNA sequences could be largely assigned to mDNA haplogroups C and D but modern European dog sequences could be largely assigned to mDNA haplogroups A and B, indicating a turnover of dogs in the past from a place other than Europe. As this split dates older than the Newgrange dog this suggests that the replacement was only partial. The analysis showed that most modern European dogs had undergone a population bottleneck which can be an indicator of travel. The archaeological record shows dog remains dating over 15,000 YBP in Western Eurasia, over 12,500 YBP in Eastern Eurasia, but none older than 8,000 YBP in Central Asia. The study proposed that dogs may have been domesticated separately in both Eastern and Western Eurasia from two genetically distinct and now extinct wolf populations. East Eurasian dogs then made their way with migrating people to Western Europe between 14,000-6,400 YBP where they partially replaced the dogs of Europe.^[16] Two domestication events in Western Eurasia and Eastern Eurasia has recently been found for the domestic pig.^[16][45]

The hypothesis proposed is that an initial wolf population split into East and West Eurasian wolves. These were then domesticated independently before becoming extinct. The Western Eurasian dog population was then partially and gradually replaced by Asian dogs that were brought by humans at least 6400 years ago.^[16] A single domestication is thought to be due to chance, however dual domestication on different sides of the world is unlikely to have happened randomly and it suggests that external factors - an environmental driver - may have forced wolves to work together with humans for survival. It is possible that wolves took advantage of resources that humans had, or humans may have been introduced to wolves in an area in which they didn’t previously live.^[59]

The study used the radiocarbon age of the Newgrange dog to calibrate the mutation rate for dogs, which was similar to that calculated for the Late Pleistocene Taimyr wolf. Comparing the sequence of the Newgrange dog using this mutation rate with two modern wolves from Russia gave a divergence time between 20,000-60,000 YBP. However, these two modern wolves may not have been closely related to the population that gave rise to the dog, which may have diverged from their ancestor at a later time.^[16]

Dog domestication

"The dog was the first domesticant. Without dogs you don't have any other domestication. You don't have civilization."^[60] "Remove domestication from the human species, and there’s probably a couple of million of us on the planet, max. Instead, what do we have? Seven billion people, climate change, travel, innovation and everything. Domestication has influenced the entire earth. And dogs were the first. For most of human history, we’re not dissimilar to any other wild primate. We’re manipulating our environments, but not on a scale bigger than, say, a herd of African elephants. And then, we go into partnership with this group of wolves. They altered our relationship with the natural world."^[61] - Greger Larson

Watercolor tracing made by archaeologist Henri Breuil from a cave painting of a wolf-like canid, Font-de-Gaume, France dated 19,000 years ago.

The domestication of animals is the scientific theory of the mutual relationship between animals with the humans who have influence on their care and reproduction.^[62] Charles Darwin recognized the small number of traits that made domestic species different from their wild ancestors. He was also the first to recognize the difference between conscious selective breeding in which humans directly select for desirable traits, and unconscious selection where traits evolve as a by-product of natural selection or from selection on other traits.^[42][63][64] There is a genetic difference between domestic and wild populations. There is also such a difference between the domestication traits that researchers believe to have been essential at the early stages of domestication, and the improvement traits that have appeared since the split between wild and domestic populations.^[7][65][66] Domestication traits are generally fixed within all domesticates, and were selected during the initial episode of domestication of that animal or plant, whereas improvement traits are present only in a proportion of domesticates, though they may be fixed in individual breeds or regional populations.^[7][66][67] The dog was the first domesticant and was established across Eurasia before the end of the Late Pleistocene era, well before cultivation and before the domestication of other animals.^[10]

See further: Domestication of animals - definitions

Time of domestication

In August 2015, a study undertook an analysis of the complete mitogenome sequences of 555 modern and ancient dogs. The sequences showed an increase in the population size approximately 23,500 YBP, which broadly coincides with the proposed separation of the ancestors of dogs and present-day wolves before the Last Glacial Maximum (refer first divergence). A ten-fold increase in the population size occurred after 15,000 YBP, which may be attributable to domestication events and is consistent with the demographic dependence of dogs on the human population (refer archaeological evidence - Eleesivich-1).^[68]

Commensal pathway

Montage showing the morphological variation of the dog.

Animal domestication is a coevolutionary process in which a population responds to selective pressure while adapting to a novel niche that included another species with evolving behaviors.^[7]

See further: Convergent evolution between dogs and humans

The dog is a classic example of a domestic animal that likely traveled a commensal pathway into domestication. The dog was the first domesticant, and was domesticated and widely established across Eurasia before the end of the Pleistocene, well before cultivation or the domestication of other animals.^[10] It may have been inevitable that the first domesticated animal came from the order of carnivores as these are less afraid when approaching other species. Within the carnivores, the first domesticated animal would need to exist without an all-meat diet, possess a running and hunting ability to provide its own food, and be of a controllable size to coexist with humans, indicating the family Canidae, and the right temperament^[69]:p166 with wolves being among the most gregarious and cooperative animals on the planet.^[70][71]

See further: Commensal pathway

Ancient DNA supports the hypothesis that dog domestication preceded the emergence of agriculture^[2][5] and was initiated close to the Last Glacial Maximum 27,000 YBP when hunter-gatherers preyed on megafauna, and when proto-dogs might have taken advantage of carcasses left on site by early hunters, assisted in the capture of prey, or provided defense from large competing predators at kill-sites.^[2] Wolves were probably attracted to human campfires by the smell of meat being cooked and discarded refuse in the vicinity, first loosely attaching themselves and then considering these as part of their home territory where their warning growls would alert humans to the approach of outsiders.^[72] The wolves most likely drawn to human camps were the less-aggressive, subdominant pack members with lowered flight response, higher stress thresholds, less wary around humans, and therefore better candidates for domestication.^[73] The earliest sign of domestication in dogs was the neotonization of skull morphology^[73][74][75] and the shortening of snout length that results in tooth crowding, reduction in tooth size, and a reduction in the number of teeth,^[50][73] which has been attributed to the strong selection for reduced aggression.^[73][74] This process may have begun during the initial commensal stage of dog domestication, even before humans began to be active partners in the process.^[7][73]

A maternal mitochondrial, paternal Y chromosome, and microsatellite assessment of two wolf populations in North America and combined with satellite telemetry data revealed significant genetic and morphological differences between one population that migrated with and preyed upon caribou, and another territorial ecotype population that remained in a boreal coniferous forest. Though these two populations spend a period of the year in the same place, and though there was evidence of gene flow between them, the difference in prey–habitat specialization has been sufficient to maintain genetic and even coloration divergence.^[7][76] A study has identified the remains of a population of extinct Pleistocene Beringian wolves with unique mitochondrial signatures. The skull shape, tooth wear, and isotopic signatures suggested these were specialist megafauna hunters and scavengers that became extinct while less specialized wolf ecotypes survived.^[7][77] Analogous to the modern wolf ecotype that has evolved to track and prey upon caribou, a Pleistocene wolf population could have begun following mobile hunter-gatherers, thus slowly acquiring genetic and phenotypic differences that would have allowed them to more successfully adapt to the human habitat.^[7][78]

Even today, the wolves on Ellesmere Island do not fear humans, which is thought to be due to them seeing humans so little, and they will approach humans cautiously, curiously and closely.^{[79][80][81][82]}

See further: Megafaunal wolf

Post-domestication gene flow

Some studies have found greater diversity in the genetic markers of dogs from East^[15][37] and Central^[14] Asia compared to Europe and have concluded that dogs originated from these regions, despite no archaeological evidence to support the conclusions.^[10] One reason for these discrepancies is the sustained admixture between different dog and wolf populations across the Old and New Worlds over at least the last 10,000 years, which has blurred the genetic signatures and confounded efforts of researchers at pinpointing the origins of dogs.^[10] Another reason is that none of the modern wolf populations are related to the Pleistocene wolves that were first domesticated.^[6] In other words, the extinction of the wolves that were the direct ancestors of dogs has muddied efforts to pinpoint the time and place of dog domestication.^[7]

See further: Post-domestication gene flow

Dog-Wolf hybridization

mDNA (maternal) ancestry of the Dog

Gray wolf Dog D D2 dog/wolf hybrid[37][68] rare Middle east[39] D1 dog/wolf hybrid[37][68] Scandinavia, wolf no match[83] ABCEF F dog/wolf hybrid rare Japan[37][68] with Japanese wolf[84] ABCE BCE C C2 C1 BE E dog/wolf hybrid rare East Asia[37][68] B B2 dog/wolf hybrid[37][68] B1 A A6 dog/wolf hybrid[37][68] A4-5 A5 dog/wolf hybrid[37][68] A4 dog/wolf hybrid[37][68] A1-3 A2-3 A3 dog/wolf hybrid[37][68] A2 dog/wolf hybrid[37][68] A1

Phylogenetic classification based on the entire mitochondrial genomes of the domestic dog. These resolve into 6 mDNA Haplogroups, most indicated as a result of male dog/female wolf hybridization.[37][68]

Phylogenetic analysis shows that modern dog mDNA haplotypes resolve into four monophyletic clades with strong statistical support, and these have been designated by researchers as clades A-D.^[2][5][44] Other studies that included a wider sample of specimens have reported two rare East Asian clades E-F with weaker statistical support.^[37][40][68] In 2009, a study found that haplogroups A, B and C included 98% of dogs and are found universally distributed across Eurasia, indicating that they were the result of a single domestication event, and that haplogroups D, E, and F were rare and appeared to be the result of regional hybridization with local wolves post-domestication. Haplogroups A and B contained subclades that appeared to be the result of hybridization with wolves post-domestication, because each haplotype within each of these subclades was the result of a female wolf/male dog pairing.^[37][68]

Haplogroup A: Includes 64-65% of dogs.^[2][68] Haplotypes of subclades a2–a6 are derived from post-domestication wolf–dog hybridization.^[37][68]

Haplogroup B: Includes 22-23% of dogs.^[2][68] haplotypes of subclade b2 are derived from post-domestication wolf–dog hybridization.^[37][68]

Haplogroup C: Includes 10-12% of dogs.^[2][68]

Haplogroup D: Derived from post-domestication wolf–dog hybridization in subclade d1 (Scandinavia) and d2 (South-West Asia).^[37][68] The northern Scandinavian subclade d1 hybrid haplotypes originated 480-3,000 YBP and are found in all Sami-related breeds: Finnish Lapphund, Swedish Lapphund, Lapponian Herder, Jamthund, Norwegian Elkhound and Hällefors Elkhound. The maternal wolf sequence that contributed to them has not been matched across Eurasia^[83] and its branch is phylogenetically rooted in the same sequence as the Altai dog (not a direct ancestor).^[2] The subclade d2 hybrid haplotypes are found in 2.6% of South-West Asian dogs.^[39]

Haplogroup E: Derived from post-domestication wolf–dog hybridization in East Asia,^[37][68] (rare distribution in South-East Asia, Korea and Japan).^[39]

Haplogroup F: Derived from post-domestication wolf–dog hybridization in Japan.^[37][68] A study of 600 dog specimens found only one dog whose sequence indicated hybridization with the extinct Japanese wolf.^[84]

It is not known whether this hybridization was the result of humans selecting for phenotypic traits from local wolf populations^[44] or the result of natural introgression as the dog expanded across Eurasia.^[10]

The Greenland dog carries 3.5% shared genetic material with the 35,000 years BP Taymyr wolf specimen.

Taimyr wolf admixture

There was admixture between Taimyr-1 and those breeds associated with high latitudes.

In May 2015, a study compared the ancestry of the Taimyr-1 wolf lineage to that of dogs and gray wolves.

Comparison to the gray wolf lineage indicated that Taimyr-1 was basal to gray wolves from the Middle East, China, Europe and North America but shared a substantial amount of history with the present-day gray wolves after their divergence from the coyote. This implies that the ancestry of the majority of gray wolf populations today stems from an ancestral population that lived less than 35,000 years ago but before the inundation of the Bering Land Bridge with the subsequent isolation of Eurasian and North American wolves.^[27]:21

A comparison of the ancestry of the Taimyr-1 lineage to the dog lineage indicated that some modern dog breeds have a closer association with either the gray wolf or Taimyr-1 due to admixture. The Saarloos wolfdog showed more association with the gray wolf, which is in agreement with the documented historical crossbreeding with gray wolves in this breed. Taimyr-1 shared more alleles (i.e. gene expressions) with those breeds that are associated with high latitudes - the Siberian husky and Greenland dog that are also associated with arctic human populations, and to a lesser extent the Shar Pei and Finnish spitz. An admixture graph of the Greenland dog indicates a best-fit of 3.5% shared material, although an ancestry proportion ranging between 1.4% and 27.3% is consistent with the data. This indicates admixture between the Taimyr-1 population and the ancestral dog population of these four high-latitude breeds. These results can be explained either by a very early presence of dogs in northern Eurasia or by the genetic legacy of Taimyr-1 being preserved in northern wolf populations until the arrival of dogs at high latitudes. This introgression could have provided early dogs living in high latitudes with phenotypic variation beneficial for adaption to a new and challenging environment. It also indicates that the ancestry of present-day dog breeds descends from more than one region.^[27]:3–4

An attempt to explore admixture between Taimyr-1 and gray wolves produced unreliable results.^[27]:23

As the Taimyr wolf had contributed to the genetic makeup of the Arctic breeds, a later study suggested that descendants of the Taimyr wolf survived until dogs were domesticated in Europe and arrived at high latitudes where they mixed with local wolves, and these both contributed to the modern Arctic breeds. Based on the most widely accepted oldest zooarchaeological dog remains, domestic dogs most likely arrived at high latitudes within the last 15,000 years. The mutation rates calibrated from both the Taimyr wolf and the Newgrange dog genomes suggest that modern wolf and dog populations diverged from a common ancestor between 20,000 and 60,000 YBP. This indicates that either dogs were domesticated much earlier than their first appearance in the archaeological record, or they arrived in the Arctic early, or both.^[13]

Positive selection

Reduction in size under domestication - grey wolf and chihuahua skulls.

Charles Darwin recognized the small number of traits that made domestic species different from their wild ancestors. He was also the first to recognize the difference between conscious selective breeding in which humans directly select for desirable traits, and unconscious selection where traits evolve as a by-product of natural selection or from selection on other traits.^[42][64] Domestic animals have variations in coat color as well as texture, dwarf and giant varieties, and changes in their reproductive cycle, and many others have tooth crowding and floppy ears.

Although it is easy to assume that each of these traits was uniquely selected for by hunter-gatherers and early farmers, beginning in 1959 Dmitri K. Belyaev tested the reactions of silver foxes to a hand placed in their cage and selected the tamest, least aggressive individuals to breed. His hypothesis was that, by selecting a behavioral trait, he could also influence the phenotype of subsequent generations, making them more domestic in appearance. Over the next 40 years, he succeeded in producing foxes with traits that were never directly selected for, including piebald coats floppy ears, upturned tails, shortened snouts, and shifts in developmental timing.^[74][85][86] In the 1980s, a researcher used a set of behavioral, cognitive, and visible phenotypic markers, such as coat colour, to produce domesticated fallow deer within a few generations.^[85][87] Similar results for tameness and fear have been found for mink^[88] and Japanese quail.^[89] In addition to demonstrating that domestic phenotypic traits could arise through selection for a behavioral trait, and domestic behavioral traits could arise through the selection for a phenotypic trait, these experiments provided a mechanism to explain how the animal domestication process could have begun without deliberate human forethought and action.^[85]

The genetic difference between domestic and wild populations can be framed within two considerations. The first distinguishes between domestication traits that are presumed to have been essential at the early stages of domestication, and improvement traits that have appeared since the split between wild and domestic populations.^[7][65][66] Domestication traits are generally fixed within all domesticates and were selected during the initial episode of domestication, whereas improvement traits are present only in a proportion of domesticates, though they may be fixed in individual breeds or regional populations.^[7][66][67] A second issue is whether traits associated with the domestication syndrome resulted from a relaxation of selection as animals exited the wild environment or from positive selection resulting from intentional and unintentional human preference. Some recent genomic studies on the genetic basis of traits associated with the domestication syndrome have shed light on both of these issues.^[7] A study published in 2016 suggested that there have been negative genetic consequences of the domestication process as well, that enrichment of disease-related gene variants accompanied positively selected traits.^[90]

In 2010, a study identified 51 regions of the dog genome that were associated with phenotypic variation among breeds in 57 traits studied, which included body, cranial, dental, and long bone shape and size. There were 3 quantitative trait loci that explained most of the phenotypic variation. Indicators of recent selection were shown by many of the 51 genomic regions that were associated with traits that define a breed, which include body size, coat characteristics, and ear floppiness.^[91] Geneticists have identified more than 300 genetic loci and 150 genes associated with coat color variability.^[85][92] Knowing the mutations associated with different colors has allowed the correlation between the timing of the appearance of variable coat colors in horses with the timing of their domestication.^[85][93] Other studies have shown how human-induced selection is responsible for the allelic variation in pigs.^[85][94] Together, these insights suggest that, although natural selection has kept variation to a minimum before domestication, humans have actively selected for novel coat colors as soon as they appeared in managed populations.^[85][95]

In 2015, a study looked at over 100 pig genome sequences to ascertain their process of domestication. A model that fitted the data included admixture with a now extinct ghost population of wild pigs during the Pleistocene. The study also found that despite back-crossing with wild pigs, the genomes of domestic pigs have strong signatures of selection at genetic loci that affect behavior and morphology. The study concluded that human selection for domestic traits likely counteracted the homogenizing effect of gene flow from wild boars and created domestication islands in the genome. The same process may also apply to other domesticated animals.^[45][96]

In 2014, a whole genome study of the DNA differences between wolves and dogs found that dogs did not show a reduced fear response but did show greater synaptic plasticity. Synaptic plasticity is widely believed to be the cellular correlate of learning and memory, and this change may have altered the learning and memory abilities of dogs in comparison to wolves.^[97]

Behavior

Unlike other domestic species which were primarily selected for production-related traits, dogs were initially selected for their behaviors.^[98][99] In 2016, a study found that there were only 11 fixed genes that showed variation between wolves and dogs. These gene variations were unlikely to have been the result of natural evolution, and indicate selection on both morphology and behavior during dog domestication. There was evidence of selection during dog domestication of genes that affect the adrenaline and noradrenaline biosynthesis pathway. These genes are involved in the synthesis, transport and degradation of a variety of neurotransmitters, particularly the catecholamines, which include dopamine and noradrenaline. Recurrent selection on this pathway and its role in emotional processing and the fight-or-flight response^[99][100] suggests that the behavioral changes we see in dogs compared to wolves may be due to changes in this pathway, leading to tameness and an emotional processing ability.^[99] Dogs generally show reduced fear and aggression compared to wolves.^[99][101] Some of these genes have been associated with aggression in some dog breeds, indicating their importance in both the initial domestication and then later in breed formation.^[99]

Dietary adaption

The difference in overall body size between a Cane Corso (Italian mastiff) and a Yorkshire terrier is over 30-fold, yet both are members of the same species.

AMY2B (Alpha-Amylase 2B) is a gene that codes a protein that assists with the first step in the digestion of dietary starch and glycogen. An expansion of this gene in dogs would enable early dogs to exploit a starch-rich diet as they fed on refuse from agriculture.^[6][99] In a study in 2014, the data indicated that the wolves and dingo had just two copies of the gene and the Siberian Husky that is associated with hunter-gatherers had just three or four copies, whereas the Saluki that is associated with the Fertile Crescent where agriculture originated had 29 copies. The results show that on average, modern dogs have a high copy number of the gene, whereas wolves and dingoes do not. The high copy number of AMY2B variants likely already existed as a standing variation in early domestic dogs, but expanded more recently with the development of large agriculturally based civilizations. This suggests that at the beginning of the domestication process, dogs may have been characterized by a more carnivorous diet than their modern-day counterparts, a diet held in common with early hunter-gatherers.^[6] A later study indicated that because most dogs had a high copy number of the AMY2B gene but the arctic breeds and the dingo did not, that the dog's dietary change may not have been caused by initial domestication but by the subsequent spread of agriculture to most - but not all - regions of the planet.^[102]

In 2016, a study of the dog genome compared to the wolf genome looked for genes that showed signs of having undergone positive selection. The study identified genes relating to brain function and behavior, and to lipid metabolism. This ability to process lipids indicates a dietary target of selection that was important when proto-dogs hunted and fed alongside hunter-gatherers. The evolution of the dietary metabolism genes may have helped process the increased lipid content of early dog diets as they scavenged on the remains of carcasses left by hunter-gatherers.^[103] Prey capture rates may have increased in comparison to wolves and with it the amount of lipid consumed by the assisting proto-dogs.^{[103][104][105]} A unique dietary selection pressure may have evolved both from the amount consumed, and the shifting composition of, tissues that were available to proto-dogs once humans had removed the most desirable parts of the carcass for themselves.^[103] A study of the mammal biomass during modern human expansion into the northern Mammoth steppe found that it had occurred under conditions of unlimited resources, and that many of the animals were killed with only a small part consumed or left unused.^[106]

See further:phenotypic plasticity

Natural selection

Dogs can infer the name of an object and have been shown to learn the names of over 1,000 objects. Dogs can follow the human pointing gesture; even nine-week-old puppies can follow a basic human pointing gesture without being taught. New Guinea singing dogs, a half-wild proto-dog endemic to the remote alpine regions of New Guinea, as well as dingoes in the remote Outback of Australia are also capable of this. These examples demonstrate an ability to read human gestures that arose early in domestication and did not require human selection. "Humans did not develop dogs, we only fine-tuned them down the road."^[107]:92

See further: Dog learning by inference

A dog's cranium is 15% smaller than an equally heavy wolf's, and the dog is less aggressive and more playful. Other species pairs show similar differences. Bonobos, like chimpanzees, are a close genetic cousin to humans, but unlike the chimpanzees, bonobos are not aggressive and do not participate in lethal inter-group aggression or kill within their own group. The most distinctive features of a bonobo are its cranium, which is 15% smaller than a chimpanzee's, and its less aggressive and more playful behavior. In other examples, the guinea pig's cranium is 13% smaller than its wild cousin the cavy, and domestic fowl show a similar reduction to their wild cousins. Possession of a smaller cranium for holding a smaller brain is a telltale sign of domestication. Bonobos appear to have domesticated themselves.^[107]:104 In the farm fox experiment, humans selectively bred foxes against aggression, causing domestication syndrome. The foxes were not selectively bred for smaller craniums and teeth, floppy ears, or skills at using human gestures, but these traits were demonstrated in the friendly foxes. Natural selection favors those that are the most successful at reproducing, not the most aggressive. Selection against aggression made possible the ability to cooperate and communicate among foxes, dogs and bonobos. Perhaps it did the same thing for humans.^{[107]:114[108]} The more docile animals have been found to have less testosterone than their more aggressive counterparts, and testosterone controls aggression and brain size. One researcher has argued that in becoming more social, we humans have developed a smaller brain than those of humans 20,000 years ago.^[109]

Convergent evolution between dogs and humans

As a result of the domestication process there is also evidence of convergent evolution having occurred between dogs and humans.^[107]

Montage showing the coat variation of the dog.

Biological evidence

In 2007, a study found that dog domestication was accompanied by selection at three genes with key roles in starch digestion: AMY2B, MGAMand SGLT1, and was a striking case of parallel evolution when coping with an increasingly starch-rich diet caused similar adaptive responses in dogs and humans.^[110][111]

In 2013, a DNA sequencing study indicated that parallel evolution in humans and dogs is most apparent in the genes for digestion and metabolism, neurological processes, and cancer, likely as a result of shared selection pressures.^[35][112]

In 2014, a study compared the hemoglobin levels of village dogs and people on the Chinese lowlands with those on the Tibetan Plateau. It found the hemoglobin levels higher for both people and dogs in Tibet, suggesting that Tibetan dogs might share similar adaptive strategies as the Tibetan people. A population genetic analysis then showed a significant convergence between humans and dogs in Tibet.^[113]

In 2015, a study found that when dogs and their owners interact, extended eye contact (mutual gaze) increases oxytocin levels in both the dog and its owner. As oxytocin is known for its role in maternal bonding, it is considered likely that this effect has supported the coevolution of human-dog bonding.^[114] One observer has stated, "The dog could have arisen only from animals predisposed to human society by lack of fear, attentiveness, curiosity, necessity, and recognition of advantage gained through collaboration....the humans and wolves involved in the conversion were sentient, observant beings constantly making decisions about how they lived and what they did, based on the perceived ability to obtain at a given time and place what they needed to survive and thrive. They were social animals willing, even eager, to join forces with another animal to merge their sense of group with the others' sense and create an expanded super-group that was beneficial to both in multiple ways. They were individual animals and people involved, from our perspective, in a biological and cultural process that involved linking not only their lives but the evolutionary fate of their heirs in ways, we must assume, they could never have imagined. Powerful emotions were in play that many observers today refer to as love – boundless, unquestioning love."^[19]

Behavioral evidence

Convergent evolution is when distantly related species independently evolve similar solutions to the same problem. For example, fish, penguins and dolphins have each separately evolved flippers as a solution to the problem of moving through the water. What has been found between dogs and humans is something less frequently demonstrated: psychological convergence. Dogs have independently evolved to be cognitively more similar to humans than we are to our closest genetic relatives.^[107]:60 Dogs have evolved specialized skills for reading human social and communicative behavior. These skills seem more flexible – and possibly more human-like – than those of other animals more closely related to humans phylogenetically, such as chimpanzees, bonobos and other great apes. This raises the possibility that convergent evolution has occurred: both Canis familiaris and Homo sapiens might have evolved some similar (although obviously not identical) social-communicative skills – in both cases adapted for certain kinds of social and communicative interactions with human beings.^[108]

The pointing gesture is a human-specific signal, is referential in its nature, and is a foundation building-block of human communication. Human infants acquire it weeks before the first spoken word.^[115] In 2009, a study compared the responses to a range of pointing gestures by dogs and human infants. The study showed little difference in the performance of 2-year-old children and dogs, while 3-year-old children's performance was higher. The results also showed that all subjects were able to generalize from their previous experience to respond to relatively novel pointing gestures. These findings suggest that dogs demonstrating a similar level of performance as 2-year-old children can be explained as a joint outcome of their evolutionary history as well as their socialization in a human environment.^[116]

Later studies support coevolution in that dogs can discriminate the emotional expressions of human faces,^[117] and that most people can tell from a bark whether a dog is alone, being approached by a stranger, playing, or being aggressive,^[118] and can tell from a growl how big the dog is.^[119]

Human adoption of some wolf behaviors

"Isn't it strange that, our being such an intelligent primate, we didn't domesticate chimpanzees as companions instead? Why did we choose wolves even though they are strong enough to maim or kill us?"^[70]

Bison surrounded by gray wolf pack

In 2002, a study proposed that immediate human ancestors and wolves may have domesticated each other through a strategic alliance that would change both respectively into humans and dogs. The effects of human psychology, hunting practices, territoriality and social behavior would have been profound.^[120] Wolves and dogs mark their territory with scent; however, humans do not have a keen sense of smell and may have begun to mark their territories with symbols, which became the first art and may have been generative of human culture.^[120][121] Wolves hunt large game; however, there is no evidence of pre-sapiens hunting large game. Early humans moved from scavenging and small-game hunting to big-game hunting by living in larger, socially more-complex groups, learning to hunt in packs, and developing powers of cooperation and negotiation in complex situations. As these are characteristics of wolves, dogs and humans, it can be argued that these behaviors were enhanced once wolves and humans began to cohabit. Communal hunting led to communal defense. Wolves actively patrol and defend their scent-marked territory, and perhaps humans had their sense of territoriality enhanced by living with wolves.^[120] One of the keys to recent human survival has been the forming partnerships. Strong bonds exist between same-sex wolves, dogs and humans and these bonds are stronger than exist between other same-sex animal pairs. Today, the most widespread form of inter-species bonding occurs between humans and dogs. The concept of friendship has ancient origins but it may have been enhanced through the inter-species relationship to give a survival advantage.^[120][122]

In 2003, a study compared the behavior and ethics of chimpanzees, wolves and humans. Cooperation among humans' closest genetic relative is limited to occasional hunting episodes or the persecution of a competitor for personal advantage, which had to be tempered if humans were to become domesticated.^[70][123] The closest approximation to human morality that can be found in nature is that of the gray wolf, Canis lupus. Wolves are among the most gregarious and cooperative of animals on the planet,^[70][71] and their ability to cooperate in well-coordinated drives to hunt prey, carry items too heavy for an individual, provisioning not only their own young but also the other pack members, babysitting etc. are rivaled only by that of human societies. Similar forms of cooperation are observed in two closely related canids, the African wild dog and the Asian dhole, therefore it is reasonable to assume that canid sociality and cooperation are old traits that in terms of evolution predate human sociality and cooperation. Today's wolves may even be less social than their ancestors, as they have lost access to big herds of ungulates and now tend more toward a lifestyle similar to coyotes, jackals, and even foxes.^[70] Social sharing within families may be a trait that early humans learned from wolves,^[70][124] and with wolves digging dens long before humans constructed huts it is not clear who domesticated whom.^[70][123]

On the mammoth steppe the wolf's ability to hunt in packs, to share risk fairly among pack members, and to cooperate moved them to the top of the food chain above lions, hyenas and bears. Some wolves followed the great reindeer herds, eliminating the unfit, the weaklings, the sick and the aged, and therefore improved the herd. These wolves had become the first pastoralists hundreds of thousands of years before humans also took to this role. The wolves' advantage over their competitors was that they were able to keep pace with the herds, move fast and enduringly, and make the most efficient use of their kill by their ability to "wolf down" a large part of their quarry before other predators had detected the kill. The authors of the study propose that during the Last Glacial Maximum, some of our ancestors teamed up with those pastoralist wolves and learned their techniques.^[70][125] Many of our ancestors remained gatherers and scavengers, or specialized as fish-hunters, hunter-gatherers, and hunter-gardeners. However, some ancestors adopted the pastoralist wolves' lifestyle as herd followers and herders of reindeer, horses, and other hoofed animals. They harvested the best stock for themselves while the wolves kept the herd strong, and this group of humans was to become the first herders and this group of wolves was to become the first dogs.^[70]

First dogs as a hunting technology

During the late Paleolithic, the increase in human population density, advances in blade and hunting technology, and climate change may have altered prey densities and made scavenging crucial to the survival of some wolf populations. Adaptations to scavenging such as tameness, small body size, and a decreased age of reproduction would reduce their hunting efficiency further, eventually leading to obligated scavenging.^[14][126] Whether these earliest dogs were simply human-commensal scavengers or they played some role as companions or hunters that hastened their spread is unknown.^[14]

Researchers have proposed that in the past a hunting partnership existed between humans and dogs that was the basis for dog domestication.^{[127][128][129]} The transition from the Late Pleistocene into the early Holocene was marked by climatic change from cold and dry to warmer, wetter conditions and rapid shifts in flora and fauna, with much of the open habitat of large herbivores being replaced by forests.^[129] In the early Holocene, it is proposed that along with changes in arrow-head technology that hunting dogs were used by hunters to track and retrieve wounded game in thick forests.^[128][129] The dog's ability to chase, track, sniff out and hold prey can significantly increase the success of hunters in forests, where human senses and location skills are not as sharp as in more open habitats. Dogs are still used for hunting in forests today.^[129]

In Japan, temperate deciduous forests rapidly spread onto the main island of Honshu and caused an adaption away from hunting megafauna (Naumann’s elephant and Yabe’s giant deer) to hunting the quicker sika deer and wild boar in dense forest. With this came a change in hunting technology, including a shift to smaller, triangular points for arrows. A study of the Jōmon people that lived on the Pacific coast of Honshu during the early Holocene shows that they were conducting individual dog burials and were probably using dogs as tools for hunting sika deer and wild boar, as hunters in Japan still do today.^[129]

Hunting dogs make major contributions to forager societies and the ethnographic record shows them being given proper names, treated as family members, and considered separate to other types of dogs.^[129][130] This special treatment includes separate burials with markers and grave-goods,^{[129][131][132]} with those that were exceptional hunters or that were killed on the hunt often venerated.^[129][133] A dog's value as a hunting partner gives them status as a living weapon and the most skilled elevated to taking on a "personhood", with their social position in life and in death similar to that of the skilled hunters.^[129][134]

Intentional dog burials together with ungulate hunting is also found in other early Holocene deciduous forest forager societies in Europe^[135] and North America,^[136][137] indicating that across the Holarctic temperate zone hunting dogs were a widespread adaptation to forest ungulate hunting.^[129]

References

1. Fan, Zhenxin; Silva, Pedro; Gronau, Ilan; Wang, Shuoguo; Armero, Aitor Serres; Schweizer, Rena M.; Ramirez, Oscar; Pollinger, John; Galaverni, Marco; Ortega Del-Vecchyo, Diego; Du, Lianming; Zhang, Wenping; Zhang, Zhihe; Xing, Jinchuan; Vilà, Carles; Marques-Bonet, Tomas; Godinho, Raquel; Yue, Bisong; Wayne, Robert K. (2016). "Worldwide patterns of genomic variation and admixture in gray wolves". Genome Research. 26 (2): 163–73. doi:10.1101/gr.197517.115. PMID 26680994.
2. Thalmann, O. (2013). "Complete mitochondrial genomes of ancient canids suggest a European origin of domestic dogs". Science. 342 (6160): 871–4. doi:10.1126/science.1243650. PMID 24233726.
3. Vila, C.; Amorim, I. R.; Leonard, J. A.; Posada, D.; Castroviejo, J.; Petrucci-Fonseca, F.; Crandall, K. A.; Ellegren, H.; Wayne, R. K. (1999). "Mitochondrial DNA phylogeography and population history of the grey wolf Canis lupus". Molecular Ecology. 8 (12): 2089–103. doi:10.1046/j.1365-294x.1999.00825.x. PMID 10632860.
4. vonHoldt, B. (2010). "Genome-wide SNP and haplotype analyses reveal a rich history underlying dog domestication". Nature. 464 (7290): 898–902. doi:10.1038/nature08837. PMC 3494089. PMID 20237475.
5. Vila, C. (1997). "Multiple and ancient origins of the domestic dog". Science. 276 (5319): 1687–9. doi:10.1126/science.276.5319.1687. PMID 9180076.
6. Freedman, A. (2014). "Genome sequencing highlights the dynamic early history of dogs". PLOS Genetics. 10 (1): e1004016. doi:10.1371/journal.pgen.1004016. PMC 3894170. PMID 24453982.
7. Larson G, Bradley DG (2014). "How Much Is That in Dog Years? The Advent of Canine Population Genomics". PLOS Genetics. 10 (1): e1004093. doi:10.1371/journal.pgen.1004093. PMC 3894154. PMID 24453989.
8. Liane Giemsch, Susanne C. Feine, Kurt W. Alt, Qiaomei Fu, Corina Knipper, Johannes Krause, Sarah Lacy, Olaf Nehlich, Constanze Niess, Svante Pääbo, Alfred Pawlik, Michael P. Richards, Verena Schünemann, Martin Street, Olaf Thalmann, Johann Tinnes, Erik Trinkaus & Ralf W. Schmitz. "Interdisciplinary investigations of the late glacial double burial from Bonn-Oberkassel". Hugo Obermaier Society for Quaternary Research and Archaeology of the Stone Age: 57th Annual Meeting in Heidenheim, 7th – 11th April 2015, 36-37
9. Germonpre, M. (2009). "Fossil dogs and wolves from Palaeolithic sites in Belgium, the Ukraine and Russia: Osteometry, ancient DNA and stable isotopes". Journal of Archaeological Science. 36 (2): 473–490. doi:10.1016/j.jas.2008.09.033.
10. Larson G (2012). "Rethinking dog domestication by integrating genetics, archeology, and biogeography". PNAS. 109 (23): 8878–8883. doi:10.1073/pnas.1203005109. PMC 3384140. PMID 22615366.
11. "Domestication". Encyclopaedia Britannica. 2016. Retrieved May 26, 2016.
12. Perri, Angela (2016). "A wolf in dog's clothing: Initial dog domestication and Pleistocene wolf variation". Journal of Archaeological Science. 68: 1. doi:10.1016/j.jas.2016.02.003.
13. Machugh, David E.; Larson, Greger; Orlando, Ludovic (2016). "Taming the Past: Ancient DNA and the Study of Animal Domestication". Annual Review of Animal Biosciences. 5. doi:10.1146/annurev-animal-022516-022747.
14. Shannon, L (2015). "Genetic structure in village dogs reveals a Central Asian domestication origin". Proceedings of the National Academy of Sciences. 112 (44): 201516215. doi:10.1073/pnas.1516215112.
15. Wang, G (2015). "Out of southern East Asia: the natural history of domestic dogs across the world". Cell Research. 26 (1): 21–33. doi:10.1038/cr.2015.147. PMC 4816135. PMID 26667385.
16. Frantz, L. A. F.; Mullin, V. E.; Pionnier-Capitan, M.; Lebrasseur, O.; Ollivier, M.; Perri, A.; Linderholm, A.; Mattiangeli, V.; Teasdale, M. D.; Dimopoulos, E. A.; Tresset, A.; Duffraisse, M.; McCormick, F.; Bartosiewicz, L.; Gal, E.; Nyerges, E. A.; Sablin, M. V.; Brehard, S.; Mashkour, M.; b l Escu, A.; Gillet, B.; Hughes, S.; Chassaing, O.; Hitte, C.; Vigne, J.-D.; Dobney, K.; Hanni, C.; Bradley, D. G.; Larson, G. (2016). "Genomic and archaeological evidence suggest a dual origin of domestic dogs". Science. 352 (6290): 1228. doi:10.1126/science.aaf3161. PMID 27257259.
17. Grimm, David (2016). "Dogs may have been domesticated more than once". Science. doi:10.1126/science.aaf5755.
18. R.M. Nowak (2003). "Chapter 9 - Wolf evolution and taxonomy". In Mech, L. David; Boitani, Luigi. Wolves: Behaviour, Ecology and Conservation. University of Chicago Press. pp. 239–258. ISBN 978-0-226-51696-7. page 239
19. Derr, M. (2011). How the Dog Became the Dog: From Wolves to Our Best Friends. Penguin Group USA. p. 40. ISBN 1-59020-700-9.
20. "Evolution". Oxford Dictionaries. Oxford University Press. 2014.
21. Darwin, 1859. On the Origin of Species, Chapter XIII
22. University of California Museum of Paleontology. "Understanding Evolution".
23. Freedman, Adam H.; Lohmueller, Kirk E.; Wayne, Robert K. (2016). "Evolutionary History, Selective Sweeps, and Deleterious Variation in the Dog". Annual Review of Ecology, Evolution, and Systematics. 47: 73. doi:10.1146/annurev-ecolsys-121415-032155.
24. Leonard, Jennifer A.; Vilà, Carles; Wayne, Robert K. (2004). "FAST TRACK: Legacy lost: Genetic variability and population size of extirpated US grey wolves (Canis lupus)". Molecular Ecology. 14 (1): 9–17. doi:10.1111/j.1365-294X.2004.02389.x. PMID 15643947.
25. Wayne, R. (1999). "Origin, genetic diversity, and genome structure of the domestic dog". BioEssays. 21 (3): 247–57. doi:10.1002/(SICI)1521-1878(199903)21:3<247::AID-BIES9>3.0.CO;2-Z. PMID 10333734.
26. Wayne, R. (1993). "Molecular evolution of the dog family". Trends in Genetics. 9 (6): 218–24. doi:10.1016/0168-9525(93)90122-X. PMID 8337763.
27. Skoglund, P. (2015). "Ancient wolf genome reveals an early divergence of domestic dog ancestors and admixture into high-latitude breeds". Current Biology. 25 (11): 1515–9. doi:10.1016/j.cub.2015.04.019. PMID 26004765.
28. Leonard, J. A.; Wayne, R. K.; Wheeler, J; Valadez, R; Guillén, S; Vilà, C (2002). "Ancient DNA Evidence for Old World Origin of New World Dogs". Science. 298 (5598): 1613–6. doi:10.1126/science.1076980. PMID 12446908.
29. Jonathan Adams. "Europe During the Last 150,000 Years". Oak Ridge National Laboratory, Oak Ridge, USA.
30. Cooper, A. (2015). "Abrupt warming events drove Late Pleistocene Holarctic megafaunal turnover". Science. 349 (6248): 602–6. doi:10.1126/science.aac4315. PMID 26250679.
31. Benazzi, S. (2011). "Early dispersal of modern humans in Europe and implications for Neanderthal behaviour". Nature. 479 (7374): 525–8. doi:10.1038/nature10617. PMID 22048311.
32. Higham, T. (2011). "The earliest evidence for anatomically modern humans in northwestern Europe". Nature. 479 (7374): 521–4. doi:10.1038/nature10484. PMID 22048314.
33. Fox, M W (1978). "11". The dog:its domestication and behavior. Garland STPM Press, New York. p. 248.
34. Manwell C.; Baker C. M. A. (1983). "Origin of the dog: From wolf or wild Canis familiaris?". Speculations in Science and Technology. 6 (3): 213–224.
35. Wang, G. (2013). "The genomics of selection in dogs and the parallel evolution between dogs and humans". Nature Communications. 4: 1860. doi:10.1038/ncomms2814. PMID 23673645.
36. "Ancient wolf genome pushes back dawn of the dog". Nature. 2015.
37. Pang, J. (2009). "mtDNA data indicate 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. doi:10.1093/molbev/msp195. PMC 2775109. PMID 19723671.
38. Ding, Z. (2011). "Origins of domestic dog in Southern East Asia is supported by analysis of Y-chromosome DNA". Heredity. 108 (5): 507–14. doi:10.1038/hdy.2011.114. PMC 3330686. PMID 22108628.
39. Ardalan, A (2011). "Comprehensive study of mtDNA among Southwest Asian dogs contradicts independent domestication of wolf, but implies dog–wolf hybridization". Ecology and Evolution. 1 (3): 373–385. doi:10.1002/ece3.35. PMC 3287314. PMID 22393507.
40. Savolainen, P. (2002). "Genetic evidence for an East Asian origin of domestic dogs". Science. 298 (5598): 1610–3. doi:10.1126/science.1073906. PMID 12446907.
41. Boyko, A. (2009). "Complex population structure in African village dogs and its implications for inferring dog domestication history". Proceedings of the National Academy of Sciences. 106 (33): 13903–13908. doi:10.1073/pnas.0902129106. PMC 2728993. PMID 19666600.
42. Darwin, Charles (1868). "Chapter 1: Domestic Dogs and Cats". The Variation of Animals and Plants under Domestication. Vol. 1. John Murray, London.
43. Pei, W. (1934). "The carnivora from locality 1 of Choukoutien". Palaeontologia Sinica, Series C, vol. 8, Fascicle 1. Geological Survey of China, Beijing. pp. 1–45.
44. Bjornerfeldt, S (2006). "Relaxation of selective constraint on dog mitochondrial DNA followed domestication". Genome Research. 16 (8): 990–994. doi:10.1101/gr.5117706. PMC 1524871. PMID 16809672.
45. Frantz, L. (2015). "Evidence of long-term gene flow and selection during domestication from analyses of Eurasian wild and domestic pig genomes". Nature Genetics. 47 (10): 1141–1148. doi:10.1038/ng.3394. PMID 26323058.
46. Lee, E. (2015). "Ancient DNA analysis of the oldest canid species from the Siberian Arctic and genetic contribution to the domestic dog". PLoS ONE. 10 (5): e0125759. doi:10.1371/journal.pone.0125759. PMC 4446326. PMID 26018528.
47. (Pitulko V.V., Kasparov A.K. Osseal Remains of Early Holocene Domestic Dogs from the Zhokhov Site (Eastern Siberian Arctic) and the Authenticity of Identifying the Ancient Canis familiaris in Archeological Excavations // Stratum plus. 2016.N 1. P.171-207
48. Boudadi-Maligne, M. (2014). "A biometric re-evaluation of recent claims for Early Upper Palaeolithic wolf domestication in Eurasia". Journal of Archaeological Science. 45: 80–89. doi:10.1016/j.jas.2014.02.006.
49. Morey, D., ed. (2010). Dogs: Domestication and the Development of a Social Bond. Cambridge University Press. p. 24. ISBN 9780521757430.
50. Turnbull Priscilla F.; Reed Charles A. (1974). "The fauna from the terminal Pleistocene of Palegawra Cave". Fieldiana: Anthropology. 63: 81–146.
51. Dikov NN (1996) The Ushki sites, Kamchatka Peninsula. American Beginnings: the Prehistory and Palaeoecology of Beringia, ed West FH (University of Chicago Press, Chicago), pp 244-250.
52. Jing Y (2010) Zhongguo gu dai jia yang dong wu de dong wu kao gu xue yan jiu (The zooarchaeology of domesticated animals in ancient China). Quaternary Sciences 30(2):298–306.
53. Leisowska, A (2015). "Autopsy carried out in Far East on world's oldest dog mummified by ice". Retrieved October 19, 2015.
54. Davis, F. (1978). "Evidence for domestication of the dog 12,000 years ago in the Natufian of Palestine". Nature. 276 (5688): 608–610. doi:10.1038/276608a0.
55. Susan J. Crockford, A Practical Guide to In Situ Dog Remains for the Field Archaeologist, 2009
56. Henriksen, B. (1976). Værdborg I: Excavations 1943-44: A Settlement of the Maglemose Culture. Copenhagen: Akademisk forlag.
57. Losey, R. (2011). "Canids as persons: Early Neolithic dog and wolf burials, Cis-Baikal, Siberia". Journal of Anthropological Archaeology. 30 (2): 174–189. doi:10.1016/j.jaa.2011.01.001.
58. Malmström, Helena; Vilà, Carles; Gilbert, M; Storå, Jan; Willerslev, Eske; Holmlund, Gunilla; Götherström, Anders (2008). "Barking up the wrong tree: Modern northern European dogs fail to explain their origin". BMC Evolutionary Biology. 8: 71. doi:10.1186/1471-2148-8-71. PMC 2288593. PMID 18307773.
59. Melissa Chan (2016). The Mysterious History Behind Humanity’s Love of Dogs (Interview with Greger Larson). Time.
60. Grimm, David (2015). "Feature: Solving the mystery of dog domestication". Science. doi:10.1126/science.aab2477. quoting Greger Larson
61. Ed Yong (2016). "A New Origin Story for Dogs - Interview with Greger Larson". The Atlantic Monthly Group.
62. Zeder MA (2015). "Core questions in domestication Research". Proceedings of the National Academy of Sciences of the United States of America. 112 (11): 3191–8. doi:10.1073/pnas.1501711112. PMC 4371924. PMID 25713127.
63. Jared Diamond (1997). Guns, Germs, and Steel. Chatto and Windus London. ISBN 978-0-09-930278-0.
64. Larson, G.; Piperno, D. R.; Allaby, R. G.; Purugganan, M. D.; Andersson, L.; Arroyo-Kalin, M.; Barton, L.; Climer Vigueira, C.; Denham, T.; Dobney, K.; Doust, A. N.; Gepts, P.; Gilbert, M. T. P.; Gremillion, K. J.; Lucas, L.; Lukens, L.; Marshall, F. B.; Olsen, K. M.; Pires, J. C.; Richerson, P. J.; Rubio De Casas, R.; Sanjur, O. I.; Thomas, M. G.; Fuller, D. Q. (2014). "Current perspectives and the future of domestication studies". Proceedings of the National Academy of Sciences. 111 (17): 6139–6146. doi:10.1073/pnas.1323964111.
65. Olsen KM, Wendel JF (2013). "A bountiful harvest: genomic insights into crop domestication phenotypes". Annu. Rev. Plant Biol. 64: 47–70. doi:10.1146/annurev-arplant-050312-120048. PMID 23451788.
66. Doust, A. N.; Lukens, L.; Olsen, K. M.; Mauro-Herrera, M.; Meyer, A.; Rogers, K. (2014). "Beyond the single gene: How epistasis and gene-by-environment effects influence crop domestication". Proceedings of the National Academy of Sciences. 111 (17): 6178–6183. doi:10.1073/pnas.1308940110.
67. Meyer, Rachel S.; Purugganan, Michael D. (2013). "Evolution of crop species: Genetics of domestication and diversification". Nature Reviews Genetics. 14 (12): 840–52. doi:10.1038/nrg3605. PMID 24240513.
68. Duleba, Anna; Skonieczna, Katarzyna; Bogdanowicz, Wiesław; Malyarchuk, Boris; Grzybowski, Tomasz (2015). "Complete mitochondrial genome database and standardized classification system for Canis lupus familiaris". Forensic Science International: Genetics. 19: 123–129. doi:10.1016/j.fsigen.2015.06.014.
69. Wang, Xiaoming; Tedford, Richard H.; Dogs: Their Fossil Relatives and Evolutionary History. New York: Columbia University Press, 2008. pp. 166
70. Schleidt, W. (2003). "Co-evolution of humans and canids: An alternative view of dog domestication: Homo homini lupus?" (PDF). Evolution and Cognition. 9 (1): 57–72.
71. Frans de Waal (2006). Primates and Philosophers: How Morality Evolved. Princeton University Press. p. 3.
72. Olsen, S. J. (1985). Origins of the domestic dog: the fossil record. Univ. of Arizona Press, Tucson, US. pp. 88–89.
73. Zeder MA (2012). "The domestication of animals". Journal of Anthropological Research. 68 (2): 161–190. doi:10.3998/jar.0521004.0068.201.
74. Lyudmila N. Trut (1999). "Early Canid Domestication: The Farm-Fox Experiment" (PDF). American Scientist. Sigma Xi, The Scientific Research Society. 87 (March–April): 160–169. Retrieved January 12, 2016.
75. Morey Darcy F (1992). "Size, shape, and development in the evolution of the domestic dog". Journal of Archaeological Science. 19 (2): 181–204. doi:10.1016/0305-4403(92)90049-9.
76. Musiani M, Leonard JA, Cluff H, Gates CC, Mariani S, et al. (2007). "Differentiation of tundra/taiga and boreal coniferous forest wolves: genetics, coat colour and association with migratory caribou". Mol. Ecol. 16 (19): 4149–70. doi:10.1111/j.1365-294x.2007.03458.x. PMID 17725575.
77. Leonard, J. (2007). "Megafaunal extinctions and the disappearance of a specialized wolf ecomorph". Current Biology. 17 (13): 1146–50. doi:10.1016/j.cub.2007.05.072. PMID 17583509.
78. Wolpert, S. (2013), "Dogs likely originated in Europe more than 18,000 years ago, UCLA biologists report", UCLA News Room, retrieved December 10, 2014
79. Arctic Wolf: The High Arctic by Laura DeLallo. Bearport Publishing, New York 2011
80. Arctic wildlife in a warming world by Michael Becker. BBC Two, 2014.
81. Ellesmere Island Journal & Field Notes by Henry Beston 2006. International Wolf Centre.
82. Arctic Wolves and Their Prey by L. David Mech. National Ocean and Atmospheric Administration, Pacific Marine Environment Laboratory, Actic Zone. 2004
83. Klutsch, C.F. (2010). "Regional occurrence, high frequency but low diversity of mitochondrial DNA haplogroup d1 suggests a recent dog-wolf hybridization in Scandinavia". Journal of Veterinary Behavior: Clinical Applications and Research. 6: 85. doi:10.1016/j.jveb.2010.08.035.
84. Ishiguro, N (2009). "Mitochondrial DNA Analysis of the Japanese Wolf (Canis Lupus Hodophilax Temminck, 1839) and Comparison with Representative Wolf and Domestic Dog Haplotypes". Zoological Science. 26 (11): 765–770. doi:10.2108/zsj.26.765. PMID 19877836.
85. Larson, G (2013). "A population genetics view of animal domestication" (PDF).
86. 6 Trut, L. et al. (2009) Animal evolution during domestication: the domesticated fox as a model. Bioessays 31, 349–360
87. Hemmer H (2005). "Neumuhle-Riswicker Hirsche: Erste planma¨ßige Zucht einer neuen Nutztierform". Naturwissenschaftliche Rundschau. 58: 255–261.
88. Malmkvist, Jen s; Hansen, Steffen W. (2002). "Generalization of fear in farm mink, Mustela vison, genetically selected for behaviour towards humans" (PDF). Animal Behaviour. 64 (3): 487–501. doi:10.1006/anbe.2002.3058.
89. Jones, R.Bryan; Satterlee, Daniel G.; Marks, Henry L. (1997). "Fear-related behaviour in Japanese quail divergently selected for body weight". Applied Animal Behaviour Science. 52: 87–98. doi:10.1016/S0168-1591(96)01146-X.
90. Marsden, Clare D.; Vecchyo, Diego Ortega-Del; O'Brien, Dennis P.; et al. (5 January 2016). "Bottlenecks and selective sweeps during domestication have increased deleterious genetic variation in dogs". Proceedings of the National Academy of Sciences of the United States of America. 113 (1): 152–7. doi:10.1073/pnas.1512501113. PMC 47118. Lay summary.
91. Boyko, Adam R.; Quignon, Pascale; Li, Lin; Schoenebeck, Jeffrey J.; Degenhardt, Jeremiah D.; Lohmueller, Kirk E.; Zhao, Keyan; Brisbin, Abra; Parker, Heidi G.; Vonholdt, Bridgett M.; Cargill, Michele; Auton, Adam; Reynolds, Andy; Elkahloun, Abdel G.; Castelhano, Marta; Mosher, Dana S.; Sutter, Nathan B.; Johnson, Gary S.; Novembre, John; Hubisz, Melissa J.; Siepel, Adam; Wayne, Robert K.; Bustamante, Carlos D.; Ostrander, Elaine A. (2010). "A Simple Genetic Architecture Underlies Morphological Variation in Dogs". PLoS Biology. 8 (8): e1000451. doi:10.1371/journal.pbio.1000451. PMID 20711490.  This article incorporates text from this source, which is in the public domain.
92. Cieslak, M. et al. (2011) Colours of domestication. Biol. Rev. 86, 885–899
93. Ludwig A.; et al. (2009). "Coat color variation at the beginning of horse domestication". Science. 324 (5926): 485. doi:10.1126/science.1172750. PMC 5102060. PMID 19390039.
94. Fang M.; et al. (2009). "Contrasting mode of evolution at a coat color locus in wild and domestic pigs". PLoS Genet. 5: e1000341. doi:10.1371/journal.pgen.1000341.
95. Hemmer, H. 1990. Domestication: The decline of environmental appreciation. Cambridge:Cambridge University Press
96. Pennisi, E. (2015). "The taming of the pig took some wild turns". Science. doi:10.1126/science.aad1692.
97. Li, Y. (2014). "Domestication of the dog from the wolf was promoted by enhanced excitatory synaptic plasticity: A hypothesis". Genome Biology and Evolution. 6 (11): 3115–21. doi:10.1093/gbe/evu245. PMC 4255776. PMID 25377939.
98. Serpell J, Duffy D. Dog Breeds and Their Behavior. In: Domestic Dog Cognition and Behavior. Berlin, Heidelberg: Springer; 2014
99. Cagan, Alex; Blass, Torsten (2016). "Identification of genomic variants putatively targeted by selection during dog domestication". BMC Evolutionary Biology. 16. doi:10.1186/s12862-015-0579-7.
100. Almada RC, Coimbra NC. Recruitment of striatonigral disinhibitory and nigrotectal inhibitory GABAergic pathways during the organization of defensive behavior by mice in a dangerous environment with the venomous snake Bothrops alternatus [ Reptilia , Viperidae ] Synapse 2015:n/a–n/a
101. Coppinger R, Schneider R: Evolution of working dogs. The domestic dog: Its evolution, behaviour and interactions with people. Cambridge: Cambridge University press, 1995
102. Arendt, M; Cairns, K M; Ballard, J W O; Savolainen, P; Axelsson, E (2016). "Diet adaptation in dog reflects spread of prehistoric agriculture". Heredity. 117 (5): 301. doi:10.1038/hdy.2016.48. PMID 27406651.
103. Freedman, Adam H.; Schweizer, Rena M.; Ortega-Del Vecchyo, Diego; Han, Eunjung; Davis, Brian W.; Gronau, Ilan; Silva, Pedro M.; Galaverni, Marco; Fan, Zhenxin; Marx, Peter; Lorente-Galdos, Belen; Ramirez, Oscar; Hormozdiari, Farhad; Alkan, Can; Vilà, Carles; Squire, Kevin; Geffen, Eli; Kusak, Josip; Boyko, Adam R.; Parker, Heidi G.; Lee, Clarence; Tadigotla, Vasisht; Siepel, Adam; Bustamante, Carlos D.; Harkins, Timothy T.; Nelson, Stanley F.; Marques-Bonet, Tomas; Ostrander, Elaine A.; Wayne, Robert K.; Novembre, John (2016). "Demographically-Based Evaluation of Genomic Regions under Selection in Domestic Dogs". PLOS Genetics. 12 (3): e1005851. doi:10.1371/journal.pgen.1005851. PMC 4778760. PMID 26943675.
104. Shipman, P. (2015). The Invaders:How humans and their dogs drove Neanderthals to extinction. Harvard University Press. ISBN 9780674736764.
105. Shipman, Pat (2015). "How do you kill 86 mammoths? Taphonomic investigations of mammoth megasites". Quaternary International. 359-360: 38–46. doi:10.1016/j.quaint.2014.04.048.
106. Zimov, S.A.; Zimov, N.S.; Tikhonov, A.N.; Chapin, F.S. (2012). "Mammoth steppe: A high-productivity phenomenon". Quaternary Science Reviews. 57: 26–45. doi:10.1016/j.quascirev.2012.10.005.
107. Hare, B. (2013). The Genius of Dogs. Penguin Publishing Group.
108. Hare B. (2005). "Human-like social skills in dogs?". Trends in Cognitive Sciences. 9 (9): 439–44. doi:10.1016/j.tics.2005.07.003. PMID 16061417.
109. Bruce Hood (psychologist) (2014). The Domesticated Brain. Pelican. ISBN 9780141974866.Preface
110. Perry, George H; Dominy, Nathaniel J; Claw, Katrina G; Lee, Arthur S; Fiegler, Heike; Redon, Richard; Werner, John; Villanea, Fernando A; Mountain, Joanna L; Misra, Rajeev; Carter, Nigel P; Lee, Charles; Stone, Anne C (2007). "Diet and the evolution of human amylase gene copy number variation". Nature Genetics. 39 (10): 1256–60. doi:10.1038/ng2123. PMC 2377015. PMID 17828263.
111. Axelsson, Erik; Ratnakumar, Abhirami; Arendt, Maja-Louise; Maqbool, Khurram; Webster, Matthew T.; Perloski, Michele; Liberg, Olof; Arnemo, Jon M.; Hedhammar, Åke; Lindblad-Toh, Kerstin (2013). "The genomic signature of dog domestication reveals adaptation to a starch-rich diet". Nature. 495 (7441): 360–4. doi:10.1038/nature11837. PMID 23354050.
112. Cossins, D. (2003), Dogs and Human Evolving Together, retrieved January 12, 2014
113. Wang, G. (2014). "Genetic convergence in the adaptation of dogs and humans to the high-altitude environment of the Tibetan Plateau". Genome Biology and Evolution. 6 (8): 2122–8. doi:10.1093/gbe/evu162. PMC 4231634. PMID 25091388.
114. Nagasawa, M. (2015). "Oxytocin-gaze positive loop and the coevolution of human-dog bonds". doi:10.1126/science.1261022.
115. Butterworth, G. (2003). "Pointing is the royal road to language for babies".
116. Lakatos, G. (2009). "A comparative approach to dogs' (Canis familiaris) and human infants' comprehension of various forms of pointing gestures". Animal Cognition. 12 (4): 621–31. doi:10.1007/s10071-009-0221-4. PMID 19343382.
117. Muller, C. (2015). "Dogs can discriminate the emotional expressions of human faces". Current Biology. 25 (5): 601–5. doi:10.1016/j.cub.2014.12.055. PMID 25683806.
118. Hare, B. (2013). "What Are Dogs Saying When They Bark?". Scientific American. Retrieved 17 March 2015.
119. Sanderson, K. (2008). "Humans can judge a dog by its growl". Nature. doi:10.1038/news.2008.852.
120. Paul Taçon, Pardoe, Colin (2002). "Dogs make us human". Nature Australia. Australian Museum. 27 (4): 52–61. also available: https://www.researchgate.net/publication/29464691_Dogs_make_us_human
121. Lyn, W.S. (2002). "'Canis Lupus Cosmopolis: Wolves in a Cosmopolitan Worldview'" (PDF). 1/3. Worldviews: 301. refer also:http://booksandjournals.brillonline.com/content/journals/10.1163/156853502320915393
122. Temple Grandin and Catherine Johnson (2005). Animals in Translation: Using the Mysteries of Autism to Decode Animal Behavior (PDF). A Harvest Book, Harcourt, Inc. New York. p. 305.
123. Kathryn Kirkpatrick (2014). Jeanne Dubino, Ziba Rashidian, Andrew Smyth, eds. Representing the Modern Animal in Culture. Palgrave McMillan New York. p. 75.
124. Fogg, Brandy R.; Howe, Nimachia; Pierotti, Raymond (2015). "Relationships Between Indigenous American Peoples and Wolves 1: Wolves as Teachers and Guides". Journal of Ethnobiology. 35 (2): 262–285. doi:10.2993/etbi-35-02-262-285.1.
125. Andrew Brown Smith (2005). African Herders: Emergence of Pastoral Traditions. Walnut Creek: Altamira Press. p. 27.
126. Coppinger R, Feinstein M (2015). How Dogs Work. University of Chicago Press, Chicago. ISBN 9780226128139.
127. Davis, S. 1982. The taming of the few. New Scientist 95: 697–700
128. Clutton-Brock, J. 1984. Dog, in I.L. Mason (ed.) Evolution of domesticated animals. London:Longman.
129. Perri, Angela R. (2016). "Hunting dogs as environmental adaptations in Jōmon Japan". Antiquity. 90 (353): 1166. doi:10.15184/aqy.2016.115.
130. Ikeya, K. 1994. Hunting with dogs among the San in the Central Kalahari. African Study Monographs 15:119–34.
131. Gron, O. & M.G. Turov. 2007. Resource ‘pooling’ and resource management. An ethno-archaeological study of the Evenk hunter-gatherers, Katanga County, Siberia, in B. Hardh, K. Jennbert & D. Olausson (ed.) On the road: studies in honour of Lars Larsson (Acta Archaeologica Lundensia 26):67–72. Stockholm: Almqvist & Wiksell.
132. Koler-Matznick, Janice; Brisbin Jr, I. Lehr; Yates, S; Bulmer, Susan (2007). "The New Guinea singing dog: its status and scientific importance". The Journal of the Australian Mammal Society. 29 (1): 47–56. doi:10.1071/AM07005.
133. Olowo Ojoade, J. 1990. Nigerian cultural attitudes to the dog, in R. Willis (ed.) Signifying animals: human meaning in the natural world: 215–21. London: Routledge.
134. Mizoguchi, K. 2002. An archaeological history of Japan: 10,000 B.C. to A.D. 700. Philadelphia: University of Pennsylvania Press.
135. Bourque, B.J. 1975. Comments on the late Archaic populations of central Maine: the view from the urner Farm. Arctic Anthropology 12: 35–45.
136. Larsson, L. 1990. Dogs in fraction—symbols in action, in P.M. Vermeersch & P. Van Peer (ed.) Contributions to the Mesolithic in Europe: 153–60. Leuven: Leuven University Press.
137. Morey, D.F. & M.D.Wiant. 1992. Early Holocene domestic dog burials from the North American Midwest. Current Anthropology 33: 224–29.

Further reading

• Gemma Tarlach (November 9, 2016). "The Origins of Dogs". Retrieved November 9, 2016.
• Mark Derr (2013). How the Dog Became the Dog: From Wolves to Our Best Friends. ISBN 978-1468302691.