Origin of the domestic dog

The origin of the domestic dog (Canis lupus familiaris or Canis familiaris) is not clear. Whole genome sequencing indicates that the dog, the gray wolf, and the extinct Taymyr wolf diverged at around the same time 27,000–40,000 years before present (YBP).^[1] These dates imply that the earliest dogs arose in the time of human hunter-gatherers and not agriculturists.^[2] Modern dogs are more closely related to ancient wolf fossils that have been found in Europe than they are to modern gray wolves,^[3] with nearly all genetic commonalities with the gray wolf due to admixture,^[2] but several Arctic dog breeds have commonalities with the Taymyr wolf of North Asia due to admixture.^[1]

Some studies have found greater diversity in the genetic markers of dogs from East^[4][5] and Central^[6] Asia compared to Europe and have concluded that dogs originated from these regions, despite no archaeological evidence to support the conclusions.^[7] 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.^[7] Another reason is that none of the modern wolf populations are related to the Pleistocene wolves that were first domesticated.^[2] 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.^[8]

Dog evolution

Dog evolution (from the Latin evolutio: "unrolling")^[9] is the biological descent with modification^[10] 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).^[11]

Genetics and archaeology

Dogs were the first domesticated taxa. When and where dogs were first domesticated has vexed geneticists for the past 20 years and archaeologists for many decades longer.^[8] 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.^[7] Today, all zooarchaeologists support the proposition that dogs were not only the first domestic animal, but that the appearance of dogs significantly predates the origins of domestic plants and early agriculture.^[8]

DNA studies may give unresolvable results due to the specimens selected, the technology used, and the assumptions made by the researchers.^[12] Any one from a panel of genetic markers can be chosen from for use in a study (for example mitochondrial Cytochrome b). The techniques used to extract, locate and compare sequences can be applied using advances in technology to observe longer lengths of base pairs that give better phylogenetic resolution.^[4] The geneticists efforts to establish the time and place of dog domestication has moved from using as tools the maternal mtDNA control region and paternal Y chromosome phylogeography, through to the short single nucleotide polymorphisms and the longer microsatellites, autosomal marker analysis, nuclear DNA analysis, and today using whole genome analysis. The challenge now is to extend the application of these technologies to ancient remains by merging the materials and methods of both archaeology and genetics and applying these to ancient DNA.^[8]

From specimen to species identification
The 33,000 year old skull of the "Altai dog"  Location of nuclear DNA within the chromosomes  The structure of part of a DNA double helix  An example of the results of automated chain-termination DNA sequencing  DNA molecule 1 differs from DNA molecule 2 at a single base-pair location - a single-nucleotide polymorphism  Phylogenetic tree and timeline towards the dog (Tedford & Wang 2009)[13]

Wolf lineage

Early DNA studies indicated that the dog is descended from a wolf lineage.

In 1868, Charles Darwin proposed that domestic dogs were phenotypically so diverse that they may have originated from two or more wild canis species.^[14]:16 All species within the Canis genus, the wolf-like canids, are phylogenetically closely related with 78 chromosomes and can potentially interbreed.^[15] Later, others thought that "the wolf is the most probable ancestor and closest relative of the domestic dog."^[16]:54

In June 1993, a study concluded that the molecular genetic evidence did not support theories that dogs arose from jackal ancestors but it did support that the dog was genetically close to the extant gray wolf. The study proposed the hypothesis that because of the diversity of dog remains found in archaeological sites, dogs may be derived from several different ancestral gray wolf populations.^[17] In 1997, a study found that no dog sequence differed from any wolf sequence by more than 12 substitutions but differed from coyote sequences by at least 20 substitutions and 2 insertions, clearly supporting a wolf ancestry for dogs. The study proposed the hypothesis that because dog haplotypes form four monophyletic clades, early domestic dogs may not have been morphologically distinct from their wild relatives until the change 10,000-15,000 YBP when humans moved from nomadic hunter-gatherer societies into agricultural societies and imposed selective regimes that resulted in marked phenotopic divergence from wolves. After the origin of dogs from a wolf ancestor, dogs and wolves may have continued to exchange genes.^[18]

In 1999, a review of the scientific literature regarding the genetic origin of the dog proposed a number of hypotheses. The molecular data indicated that dogs have protein alleles in common with wolves, share highly polymorphic microsatellites, and have mitochondrial DNA sequences similar or identical to those found in gray wolves. The mitochondrial control region DNA sequences show an average divergence between dogs and wolves of 1.5%, compared to dogs and coyotes, their next-closest relative, at 7.5%. Therefore, this indicated that the origin of the dog was from wolves. The archaeological record suggests that dogs were in Europe and the Middle East approximately 14,000 YBP, but the genetic record shows 135,000 YBP, which indicates that the morphological change was associated with artificial selection as humans shifted from hunter-gatherer to agrarian societies. Alternately, dogs may have had a more recent origin but are descended from a now extinct species of canid whose closest living relative was the gray wolf. The DNA sequences of dogs form four distinct clades, each with a separate ancestry from wolves that indicates four separate domestication events. One of the clades shows a wolf sequence that is identical to a dog sequence, suggesting a very recent interbreeding or domestication event. Once dogs were domesticated and spread over a wide area, occasional interbreeding would have transferred wolf mDNA to them.^[15]

See further: Genetic admixture

Time of divergence

The ancestral dog and the ancestral modern gray wolf diverged from a common ancestor up to 40,000 years ago.

Paleoecology

The dog came into being towards the last peak of the last Ice Age, in very cold and dry climatic conditions.

During the peak of the last Ice Age - known as the last glacial maximum - a vast mammoth steppe stretched from Spain 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 was almost non-existent, except for isolated pockets in the mountain ranges of southern Europe.^[19] 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 also involve 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 their predators.^[20] Modern humans' ancestors first reached Europe with their remains dated 43,000-45,000 years BP discovered in Italy^[21] and in Britain.^[22]

Into this environment came the dog.

See further: Paleoecology at this time

Divergence

Based on mutation rate assumptions, early mtDNA control region analysis indicated that if the dog had descended from the extant gray wolf then the divergence would have occurred 135,000 YBP.^[18] Two later studies using whole genome sequencing and mutation rate assumptions derived divergence times of 32,000 YBP,^[23] and 11,000-16,000 YBP with the assumed mutation rate "the dominant source of uncertainty in dating the origin of dogs."^[2]

In May 2015, a study was conducted on a partial rib-bone of a wolf specimen (named 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 of the nuclear genome of a Pleistocene carnivore, and the sequence was deposited in the European Nucleotide Archive and classified as Canis lupus.^[1]

Using the Taimyr-1 specimen's radiocarbon date, its genome sequence and that of a modern wolf, a direct estimate of the genome-wide mutation rate in dogs/wolves could be made to calculate the time of divergence. The data indicated that the Taimyr-1 lineage was separate to modern wolves and dogs and indicated that the Taimyr-1 genotype, 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. The separation of the dog and wolf did not have to coincide with selective breeding by humans.^{[1]:page3[24]} 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.^[1]

See also: Cladogenesis

Place of divergence

Modern dogs show a closer genetic association with ancient, extinct canids from Europe^[3]

Based on modern DNA

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.^[25] In 2011, a study found that there had been dog-wolf hybridization and not an independent domestication.^[2][26]

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.^[4] 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.^[27]

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.^[6]

See further: Altai dog – 33,000 BP

Southern 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,^[28] but this was rebutted because village dogs in Africa also show a similar haplotype diversity.^[12] 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.^[5] A criticism of the Southern East Asia proposal is that no wolf remains have been found in this region nor dog remains dated beyond 12,000 YBP, however archaeological studies in the Far East are generally lagging behind those in Europe.^[7]

Based on ancient DNA

Genetic studies comparing the dog with extant gray wolves did not result in agreement among researchers. In 1868, Charles Darwin wrote that some authors at the time proposed an unknown or extinct species was the ancestor of the dog.^[14] In 1934, an eminent paleontologist indicated that the ancestor of the dog lineage may have been the extinct Canis lupus variabilis.^[29] 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.^[15] 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 ancient DNA.^[7]

Europe: In November 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.^[3][18][30] In 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.^[3] The data supports the hypothesis that dog domestication preceded the emergence of agriculture^[18] and was initiated close to the Last Glacial Maximum when hunter-gatherers preyed on megafauna.^[3]

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.^[5] 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.^[7]

Arctic North-East Siberia: In 2015, a study looked at the mitogenome contol region sequences of 13 ancient canid remains and one modern wolf from five sites across Arctic north-east Siberia. The 14 canids revealed nine haplotypes, three of which were on record and the others unique. Four of the Siberian canids dated 28,000 YBP, and one Canis c.f. variabilis dated 360,000 YBP, were as divergent as the ancient European specimens found in an earlier study, and the European origin of domestic dogs may not be conclusive. The phylogenetic relationship of the extracted sequences showed that the haplotype from specimen S805 (28,000 YBP) was one step away from another haplotype S902 (8,000 YBP) that represents the domestic dog lineages. Several ancient haplotypes were oriented around S805, including Canis c.f. variabilis (360,000 YBP), Belgium (36,000 YBP - the "Goyet dog") and Belgium (30,000 YBP), and Konsteki, Russia (22,000 YBP). Given the position of the S805 haplotype, it may potentially represent a direct link from the putative progenitor (including Canis c.f. variabilis) to the domestic dog and modern wolf lineages.^[31]

See further: Hybrid speciation and Introgression

Probable ancestor

During the LGM, there were two types of wolf. A large, heavily-built megafaunal wolf spanned the cold north of the Holarctic that specialised in preying on megafauna. Another more gracile form lived in the warmer south in refuges from the glaciation. When the planet warmed and the LGM came to an end, whole species of megafauna became extinct along with their predators, leaving the more gracile form to dominate the Holarctic. This wolf we know today as the modern gray wolf, which is the dog's sister but not its ancestor - the dog shows a closer genetic relationship with the extinct megafaunal wolf.

Canis Divergence

Golden jackal 1.9 million YBP[32] African golden wolf 1.3 million YBP[32] Coyote 1.1 million YBP[32] Himalayan wolf 630,000 YBP[33] Indian gray wolf 270,000 YBP[33] Gray wolf (haplogroups 1 & 2)[34] Dog 40,000 YBP[1]

Lineage and divergence times

Within the species Canis lupus, phylogenetic analysis strongly supports the hypothesis that dogs and gray wolves are reciprocally monophylic taxa that form two sister clades.^{[2]:4[18]:1687}

In 2010, a study compared the mDNA haplotypes of 947 modern gray wolves from across Europe with the published sequences of 24 Pleistocene wolves from western Europe dated between 1,200-44,000 years BP. The study found that phylogenetically the haplotypes represented two haplogroups and referred to these as haplogroup 1 and 2. The 947 European wolves revealed 27 different haplotypes with haplogroup 1 forming a monophyletic clade, and all other haplotypes forming haplogroup 2. Comparison with gray wolves from other regions revealed that haplogroups 1 and 2 could be found spread across Eurasia, but only haplogroup 1 could be found in North America. The Pleistocene wolf samples from western Europe all belonged to haplogroup 2, which suggested a long-term predominance in this region. A comparison of current and past frequencies indicated that in Europe haplogroup 2 became outnumbered by haplogroup 1, but in North America haplogroup 2 became extinct and was replaced by haplogroup 1 after the Last Glacial Maximum.^[34] Access into North America was available between 20,000-11,000 years ago, after the Wisconsin glaciation had retreated but before the Bering land bridge became inundated by the sea.^[35] Therefore, haplogroup 1 was able to enter into North America during this period.

Analysis of stable isotopes, which offer conclusions about the diet and therefore the ecology of the extinct wolf populations, suggest that the Pleistocene wolves from haplogroup 2 mainly preyed on Pleistocene megafaunal species,^[36][37] which became rare at the beginning of the Holocene 12,000 years ago.^[38]:2 "Thus, Pleistocene wolves across Northern Eurasia and America may actually have represented a continuous and almost panmictic population that was genetically and probably also ecologically distinct from the wolves living in this area today."^[39]:R610 "The Pleistocene Eurasian wolves are morphologically and genetically comparable to the Pleistocene eastern-Beringian wolves."^[40]:791 Some of the ancient European and Beringian wolves shared a common haplotype (a17).^[34]:8 The specialized Pleistocene wolves, thus, did not contribute to the genetic diversity of modern wolves. Rather, modern wolf populations across the Holarctic are likely be the descendants of wolves from populations that came from more southern refuges as suggested previously^[41] for the North American wolves.^[39]:R611

These two haplogroups exclude the older-lineage Himalayan wolf and the Indian gray wolf.

The fossil remains of the direct ancestor of the dog have yet to be found, and so the probable ancestor is not confirmed.

Ancestral dog

In 1978, a researcher proposed that due to their similar behavior patterns that the dog and wolf shared a common ancestor prior to the dog's domestication, and that the "dog was the dog before it was domesticated".^[42] In 1983, a study proposed that the ancestor of Canis familiaris was a wild Canis familiaris.^[43]

Goyet dog – 36,000 BP

Genus Canis, species indeterminate

In 2009, a study looked at 117 skulls of recent and fossil large canids. None of the 10 canid skulls from the Belgian caves of Goyet, Trou du Frontel, Trou de Nutons, and Trou de Chaleux could be classified, so the team took as their basic assumption that all of these canid samples were wolves.^[44] The DNA sequence of seven of the skulls indicated seven unique haplotypes that represented ancient wolf lineages lost until now. The osteometric analysis of the skulls showed that one large canid fossil from Goyet was clearly different from recent wolves, resembling most closely the Eliseevichi-1 dogs (15,000 years YBP) and so was identified as a Paleolithic dog (see below).^[37][45]

In November 2013, a DNA study sequenced three haplotypes from the ancient Belgium canids (the Goyet dog - Belgium 36,000 YBP cataloged as Canis species, and with Belgium 30,000 YBP and 26,000 years YBP cataloged as Canis lupus) and found they formed the most diverging group. Although the cranial morphology of the Goyet dog has been interpreted as dog-like, its mitochondrial DNA relation to other canids places it as an ancient sister-group to all modern dogs and wolves rather than a direct ancestor. Belgium 26,000 YBP has been found to be uniquely large but was found not to be related to the Beringian wolf. This Belgium canid clade may represent a phenotypically distinct and not previously recognized population of gray wolf, or the Goyet dog may represent an aborted domestication episode.^[3]

Altai dog – 33,000 BP

Genus Canis, species indeterminate

In 2011, a study looked at the well-preserved 33,000-year-old skull and left mandible of a dog-like canid that was excavated from Razboinichya Cave in the Altai Mountains of southern Siberia (Central Asia). The morphology was compared to the skulls and mandibles of large Pleistocene wolves from Predmosti, Czech Republic, dated 31,000 YBP, modern wolves from Europe and North America, and prehistoric Greenland dogs from the Thule period (1,000 YBP or later) to represent large-sized but unimproved fully domestic dogs. "The Razboinichya Cave cranium is virtually identical in size and shape to prehistoric Greenland dogs" and not the ancient nor modern wolves. However, the lower carnassial tooth fell within the lower range of values for prehistoric wolves and was only slightly smaller than modern European wolves, and the upper carnassial tooth fell within the range of modern wolves. "We conclude, therefore, that this specimen may represent a dog in the very early stages of domestication, i.e. an incipient dog, rather than an aberrant wolf... The Razboinichya Cave specimen appears to be an incipient dog...and probably represents wolf domestication disrupted by the climatic and cultural changes associated with the Last Glacial Maximum".^[46]

In March 2013, a DNA study of the Altai dog deposited the sequence in GenBank with a classification of Canis lupus familiaris (dog). "The analyses revealed that the unique haplotype of the Altai dog is more closely related to modern dogs and prehistoric New World canids than it is to contemporary wolves... This preliminary analysis affirms the conclusion that the Altai specimen is likely an ancient dog with shallow divergence from ancient wolves. These results suggest a more ancient history of the dog outside of the Middle East or East Asia." The haplotype groups closest to the Altai dog included such diverse breeds as the Tibetan mastiff, Newfoundland, Chinese crested, cocker spaniel and Siberian husky.^[47]

In November 2013, a study looked at 18 fossil canids and compared these with the complete mitochondrial genome sequences from 49 modern wolves and 77 modern dogs. A more comprehensive analysis of the complete mDNA found that the phylogenetic position of the Altai dog as being either dog or wolf was inconclusive and cataloged its sequence as Canis species. All tests showed it to fall equally in both the wolf and dog clades. The sequence strongly suggests a position at the root of a clade uniting two ancient wolf genomes, two modern wolves, as well as two dogs of Scandinavian origin. However, the study does not support its recent common ancestry with the great majority of modern dogs. The study suggests that it may represent an aborted domestication episode.^[3]

Paleolithic dog – 27,000 BP

Detailed DNA analysis yet to be conducted

In 2002, a study looked at the fossil skulls from two large canids dated at 13,905 YBP that had been found buried within metres of what was once a mammoth-bone hut at the Upper Paleolithic site of Eliseevichi-1 in the Bryansk region of central Russia, and using an accepted morphologically-based definition of domestication declared them to be "Ice Age dogs".^[48] In 2013, a study re-calibrated the age of the Eliseevichi-1 specimens to 15,000 YBP and classified them as Canis lupus familiaris(dog).^[3] In 2009, a study looked at these two early dog skulls 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. The study proposed, based on the genetic evidence of the timeline and European location, the archaeological evidence of the Paleolithic dog remains being found at known European hunting camp-sites, and based on morphology and collagen analysis that showed their diet had been restricted compared to wolves, that the Paleolithic dog was domesticated. The study hypothesized that the Paleolithic dogs may have provided the stock from which early dogs came, or alternatively that they are a type of wolf that is not known to science.^[37]

See also Paleolithic dog.

Admixture

Dog-Wolf hybridization

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.^[3][18][30] Other studies that included a wider sample of specimens have reported two rare East Asian clades E-F with weaker statistical support.^[4][28][49] 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.^[4][49]

mDNA (maternal) ancestry of the Dog

Gray wolf Dog D D2 dog/wolf hybrid[4][49] rare Middle east[26] D1 dog/wolf hybrid[4][49] Scandinavia, wolf no match[50] ABCEF F dog/wolf hybrid rare Japan[4][49] with Japanese wolf[51] ABCE BCE C C2 C1 BE E dog/wolf hybrid rare East Asia[4][49] B B2 dog/wolf hybrid[4][49] B1 A A6 dog/wolf hybrid[4][49] A4-5 A5 dog/wolf hybrid[4][49] A4 dog/wolf hybrid[4][49] A1-3 A2-3 A3 dog/wolf hybrid[4][49] A2 dog/wolf hybrid[4][49] 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.[4][49]

Haplogroup A: Includes 64-65% of dogs.^[3][49] Haplotypes of subclades a2–a6 are derived from post-domestication wolf–dog hybridization.^[4][49]

Haplogroup B: Includes 22-23% of dogs.^[3][49] haplotypes of subclade b2 are derived from post-domestication wolf–dog hybridization.^[4][49]

Haplogroup C: Includes 10-12% of dogs.^[3][49]

Haplogroup D: Derived from post-domestication wolf–dog hybridization in subclade d1 (Scandinavia) and d2 (South-West Asia).^[4][49] 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 and Norwegian Elkhound. The maternal wolf sequence that contributed to them has not been matched across Eurasia^[50] and its branch is phylogenetically rooted in the same sequence as the Altai dog (not a direct ancestor).^[3] The subclade d2 hybrid haplotypes are found in 2.6% of South-West Asian dogs.^[26]

Haplogroup E: Derived from post-domestication wolf–dog hybridization in East Asia,^[4][49] (rare distribution in South-East Asia, Korea and Japan).^[26]

Haplogroup F: Derived from post-domestication wolf–dog hybridization in Japan.^[4][49] A study of 600 dog specimens found only one dog whose sequence indicated hybridization with the extinct Japanese wolf.^[51]

It is not known whether this hybridization was the result of humans selecting for phenotypic traits from local wolf populations^[30] or the result of natural introgression as the dog expanded across Eurasia.^[7]

Gray wolf admixture

There was admixture between the ancestral dog, the ancestral modern gray wolf, and the golden jackal.

The ancestral dog triverged into the dingo, Basenji and boxer lineages, and the ancestral modern gray wolf split into today's gray wolves.

In January 2014, a study analysed the whole-genome sequences of three wolves (Canis lupus) to represent the regions of Eurasia where domestication has been hypothesized to have taken place – Croatia (Europe), Israel (Middle East), and China (East/South-East Asia), plus an Australian dingo and a Basenji, being divergent lineages to the reference boxer genome, and so maximize the odds to capture distinct alleles present in the earliest dogs. These lineages are also geographically distinct, with modern Basenjis tracing their ancestry to hunting dogs of western Africa, while dingoes are free-living semi-feral dogs of Australia that arrived there at least 3,500 years ago. The natural range of wolves has never extended this far south, and due to geographic isolation they are less likely to have overlapped and admixed with wolves in the recent past. For some analyses, data were leveraged from a companion study of 12 additional dog breeds.^[2]

The data provided significant evidence of admixture between the Israeli wolf and the Basenji, the Israeli wolf and the boxer, and between the Chinese wolf and dingo. The Chinese wolf with dingo likely represents ancient admixture in Eastern Eurasia, and the Israeli wolf with Basenji and boxer likely represents ancient admixture in Western Eurasia. The fact that these lineages have been geographically isolated from wolves in the recent past suggests that this gene flow was ancestral and has likely affected most dog lineages. There was significant gene flow between the golden jackal and the Israeli wolf, as well as the population ancestral to the dog and wolf samples.^[2]

One test indicated that dogs and modern wolves form sister clades, meaning that the dog is a sister to the modern wolf and they share a common ancestor. Supporting this, another test indicated that none of the sampled wolf populations is more closely related to dogs than any of the others, and dogs diverged from wolves at about the same time as wolves diverged from each other. This implies that the wolf population(s) from which dogs originated has gone extinct and the current wolf diversity from each region represents novel, younger wolf lineages.^[2]

The data indicate that the golden jackal and the ancestor of the wolf/dog diverged 400,000 years ago. Dogs and wolves then diverged into the ancestral dog and the ancestral modern gray wolf. The ancestral modern gray wolf population triverged into the three populations studied. Not long after, the ancestral dog populations diverged into the dingo lineage, the basenji lineage and the reference boxer lineage. There was a 16-fold population bottleneck for dogs since this divergence.^[2]

There was a three-fold population decline for the three wolf samples since divergence, and it appears to have occurred well in advance of direct extermination campaigns by humans and within the timeframe of environmental and biotic changes associated with the ending of the Pleistocene era, namely changes in climate and prey, including megafaunal extinctions. This indicates that before the divergence of dogs from wolves there was much more wolf diversity. The results support a recent divergence between dogs and wolves followed by a dramatic reduction in population size.^[2]

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. 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.^[2]

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.^[1]: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.^[1]:3–4

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

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).^[49]

Dog domestication

"The dog was the first domesticant. Without dogs you don't have any other domestication. You don't have civilization."^[52]

Definitions

Domestication

Domestication (from the Latin domesticus) means "belonging to the house".^[53] Domestication has been defined as "a sustained multi-generational, mutualistic relationship in which one organism assumes a significant degree of influence over the reproduction and care of another organism in order to secure a more predictable supply of a resource of interest, and through which the partner organism gains advantage over individuals that remain outside this relationship, thereby benefitting and often increasing the fitness of both the domesticator and the target domesticate."^[54] This definition recognizes both the biological and the cultural components of the domestication process and the impacts on both humans and the domesticated animals and plants. All past definitions of domestication have included a relationship between humans with plants and animals, but their differences lay in who was considered as the lead partner in the relationship. This new definition recognizes a mutualistic relationship in which both partners gain benefits. Domestication has vastly enhanced the reproductive output of crop plants, livestock, and pets far beyond that of their wild progenitors. Domesticates have provided humans with resources that they could more predictably and securely control, move, and redistribute, which has been the advantage that had fueled a population explosion of the agro-pastoralists and their spread to all corners of the planet.^[55]

This biological mutualism is not restricted to humans with domestic crops and livestock but is well-documented in nonhuman species, especially among a number of social insect domesticators and their plant and animal domesticates, for example the ant–fungus mutualism that exists between leafcutter ants and certain fungii.^[54]

Domestication syndrome

Domestication syndrome is a term often used to describe the suite of phenotypic traits arising during domestication that distinguish crops from their wild ancestors.^[56][57] The term was later applied to animals and includes increased docility and tameness, coat color changes, reductions in tooth size, changes in craniofacial morphology, alterations in ear and tail form (e.g., floppy ears), more frequent and non-seasonal estrus cycles, alterations in adrenocorticotropic hormone levels, changed concentrations of several neurotransmitters, prolongations in juvenile behavior, and reductions in both total brain size and of particular brain regions.^[58]

Archaeological evidence

Archaeological evidence locates the earliest dog remains along with human remains 15,000 years ago at the Eliseevich-I Upper Paleolithic site, Russian Plain, Europe. 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.^[59]

Years BP	Location	Finding
400,000	Eurasia	Lower Paleolithic sites including Boxgrove near Kent, England (400,000 years BP), Zhoukoudian in North China (300,000 BP), and Lazeret in southern France (150,000 years BP) have yielded wolf bones in close association with hominid bones. "The sites of occupation and hunting activities of humans and wolves must often have overlapped."[60] We do not know if the co-location was the result of coincidence or a relationship.
200,000	Zhoukoudian cave system, China	Small, extinct wolf skulls – Canis lupus variabilis. The skull differs from the typical wolf in much smaller size with a more slender muzzle and noticeably reduced or absent sagittal crest. In addition, the lower border of some Canis lupus variabilis mandibles is "strongly convex as in the dog".[29]:15 More recent researchers have proposed that Canis lupus variabilis may be an ancestor of the dog lineage.[61][62]:7 At the site, the small wolf's remains were in close proximity to Peking man (Homo erectus pekinensis). In 2015, a mitochondrial DNA analysis was conducted on 14 ancient canid remains from Arctic Siberia and suggests a genetic contribution from regional sources of wolves, including possibly Canis cf. variabilis, to the modern dog lineage. This was the first study to extract DNA material from Canis variabilis, and it was thought to be widespread across Eurasia until 300,000 years ago.[31]
26,000	Chauvet Cave, Vallon-Pont-d'Arc, Ardèche region, France	50-metre trail of footprints made by a boy of about ten years of age alongside those of a large canid. The size and position of the canid's shortened middle toe in relation to its pads indicates a dog rather than a wolf. The footprints have been dated by soot deposited from the torch the child was carrying. The cave is famous for its cave paintings.[63]
15,000	Eliseevich-I site, Russian Plain, Russia	Two fossil dog skulls. In 2002, a study looked at the fossil skulls of two large canids that had been found buried within metres of what was once a mammoth-bone hut at the Upper Paleolithic site of Eliseevichi-1 in the Bryansk region of central Russia, and using an accepted morphologically-based definition of domestication declared them to be "Ice Age dogs".[48] The Eliseevichi-1 skull is very similar in shape to the Goyet skull (36,000 BP), the Mezine dog skull (13,500 BP) and Mezhirich dog skull (13,500 BP). In 2013, the DNA sequence was identified as Canis lupus familiaris i.e. dog.[3] See Paleolithic dog.
14,700	Bonn-Oberkassel, Germany	Dog mandible. Directly associated with a human double grave of a 50-year-old man and a 20-25-year-old woman.[64] In 2013, the DNA sequence was identified as Canis lupus familiaris i.e. dog.[3]
13,500 approx	Mezine, Ukraine	Ancient dog skull as well as ancient wolf specimens found at the site. Dated to the Epigravettian period (17,000–10,000 BP). The Mezine skull is very similar in shape to the Goyet skull (36,000 BP), Eliseevichi-1 dog skulls (15,000) and Mezhirich dog skull (13,500 BP). The Epigravettian Mezine site is well known for its round mammoth bone dwelling.[37]
13,500 approx	Mezhirich, Ukraine	Ancient dog skull. Dated to the Epigravettian period (17,000–10,000 BP). The Mezhirich skull is very similar in shape to the Goyet skull (36,000 BP), the Eliseevichi-1 dog skulls (15,000) and Mezine dog skull (13,500 BP). The Epigravettian Mazhirich site has four mammoth bone dwellings present.[37]
12,500	Kartstein cave, Mechernich, Germany	Ancient dog skull. In 2013, the DNA sequence was identified as Canis lupus familiaris i.e. dog.[3]
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.[65]
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.[66]
9,200	Texas, USA	Dog bone fragment. Found in Hinds Cave in southwest Texas. In 2011, the DNA sequence was identified as Canis lupus familiaris i.e. dog, whose ancestry was rooted in Eurasia.[67]
8,000	Svaerdborg site, Denmark	Three different dog types recorded at this Maglemosian culture site.[68]
7,800	Jiahu site, China	Eleven dog interments. Jaihu is a Neolithic site 22 kilometers north of Wuyang in Henan Province.[69]
7,425	Baikal region, Siberia, Russia	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.[70]
5,250	Skateholm, Sweden	Cemeteries contained dogs among humans. Generally, adults were buried in the central area with children and dogs in the outer area. In some cases adults, children and dogs were buried together as if forming a family. Dogs were buried with the same artifacts as humans - red ochre, flint tools or red deer antler. A dog burial with an antler head-dress and three flint blades was recovered at one of the sites.[71]:36
1,500	Dionisio Point, Galiano Island, Canada	Dogs buried in association with human burials. Two settlements with plank houses surrounded by midden. Dog remains have been recovered from the house areas and associated with human burials, and others found carefully buried within the midden which may have been a highly-symbolic place.[72]

Universal features of domesticated animals

Domestication is a fluid and nonlinear process that may start, stop, reverse, or go on unexpected paths with no clear or universal threshold that separates the wild from the domestic. However, there are universal features held in common by all domesticated animals.^[55]

Behavioral preadaption

Some animal species, and some populations within those species, make better candidates for domestication than others because they show certain behaviors: (1) large social groups with a hierarchical structure; (2) the degree of selectivity in their choice of mates and the ease of replacing one preferred partner with another; (3) the ease and speed that parents bonds with young, and the maturity and mobility of the young at birth; (4) the degree of flexibility in diet and habitat tolerance; and (5) responses to humans and new environments, including flight responses and reactivity to external stimuli.^{[55]:Fig 1[73][74][75]} Reduced wariness to humans and low reactivity to both humans and other external stimuli are a key preadaptation for domestication, and these behaviors are the main target of selection during domestication.^[8][55] This implies that not all animals can be domesticated, for example a wild member of the horse family, the Zebra.^[8][76]

Brain size and function

The sustained selection for lowered reactivity among animal domesticates has resulted in changes in brain form and function. The larger the size of the brain to begin with, and the greater its degree of folding, the greater the degree of brain-size reduction under domestication.^[55][77] Foxes that had been selectively bred for tameness over 40 years had experienced a significant reduction in cranial height and width and by inference in brain size,^[55][78] which supports the hypothesis that brain-size reduction is an early response to the selective pressure for tameness and lowered reactivity that is the universal feature of animal domestication.^[55] The most affected portion of the brain in domestic mammals is the limbic system, which in domestic dogs, pigs, and sheep show a 40% reduction in size compared with their wild species. This portion of the brain regulates endocrine function that influences behaviors such as aggression, wariness, and responses to environmentally induced stress - the key attributes of domestic animals.^[55][77]

Pleiotropy

Pleiotropy occurs when one gene influences two or more seemingly unrelated phenotypic traits. These linked traits include the animal passing through fewer development stages so that as an adult it resembles a juvenile form of its ancestor.^[55][79] Pedomorphosis in development can result in a neotonization of skull morphology, making the animal a more attractive and tractable domestic companion. Lop ears may be caused by neotonization that essentially freezes the formation of cartilage in the ears at a more juvenile stage.^[55][78] Piebald or spotted coat coloration may be caused by a linkage in the biochemical pathways of melanins (involved in coat coloration) and neurotransmitters (dopamine) that help shape behavior and cognition.^[55][80] These linked traits may arise from mutations in only a few key regulatory genes,^[55][81] and these genes can have a major impact on a network of linked genes that result in major phenotypic changes. A similar mechanism controls some of the responses of plants to domestication.^[55][82]

Limited reversion

Feral dogs, cats, goats, donkeys, pigs, and ferrets that have lived apart from humans for generations show no sign of regaining the brain mass of their wild progenitors,^[55][83] and dingoes that have lived apart from humans for thousands of years have the same brain size as a domestic dog.^[55][84] Feral dogs that actively avoid human contact are still dependent on the human niche for survival and have not reverted to the self-sustaining behaviors of their wolf ancestors.^[55][85]

Domestication pathways

Since 2012, a multi-stage model of animal domestication has been accepted by two groups. The first group proposed that animal domestication was a slow, gradually intensifying relationship between humans and animals that proceeded along a continuum of stages from anthropophily, commensalism, control in the wild, control of captive animals, extensive breeding, intensive breeding, and finally to pets.^[86][87][88]

The second group proposed that there were three major pathways that most animal domesticates followed into domestication: (1) commensals, adapted to a human niche (e.g. dogs, cats, fowl, possibly pigs); (2) prey animals sought for food (e.g. sheep, goats, cattle, water buffalo, yak, pig, reindeer, llama and alpaca); and (3) targeted animals for draft and nonfood resources (e.g. horse, donkey, camel).^{[55][89][8][88]} The beginnings of animal domestication involved a protracted coevolutionary process with multiple stages along different pathways. Humans did not envision a domesticated animal resulting from either the commensal or prey pathways. In both of these cases, humans became entangled with these species as the relationship between them, and the human role in their survival and reproduction, intensified.^[8] Although the directed pathway proceeded from capture to taming, the other two pathways are not as goal-oriented and archaeological records suggest that they take place over much longer time frames.^[87]

Commensal pathway

The commensal pathway was traveled by animals that fed on refuse around human habitats or by animals that preyed on other animals drawn to human camps. Those animals established a commensal relationship with humans in which the animals benefited but the humans received no harm but little benefit. Those animals that were most capable of taking advantage of the resources associated with human camps would have been the tamer, less aggressive individuals with shorter fight or flight distances.^[90][91][92] Later, these animals developed closer social or economic bonds with humans that lead to a domestic relationship.^[55][8][88] The leap from a synanthropic population to a domestic one could only have taken place after the animals had progressed from anthropophily to habituation, to commensalism and partnership, when the relationship between animal and human would have laid the foundation for domestication, including captivity and human-controlled breeding. From this perspective, 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.^[8]

Commensal pathway animals include dogs, cats, fowl, and possibly pigs. 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.^[7] Ancient DNA supports the hypothesis that dog domestication preceded the emergence of agriculture^[18][3] 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.^[3] 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.^[55] The earliest sign of domestication in dogs was the neotonization of skull morphology^[93][78][55] and the shortening of snout length that results in tooth crowding, reduction in tooth size, and a reduction in the number of teeth,^[94][55] which has been attributed to the strong selection for reduced aggression.^[78][55] This process may have begun during the initial commensal stage of dog domestication, even before humans began to be active partners in the process.^[55][8]

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.^[95][8] 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 went extinct while less specialized wolf ecotypes survived.^[36][8] 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.^[96][8]

See further: Megafaunal wolf

Against this proposition, at the time of domestication near the Last Glacial Maximum humans were already the top predator and had no need for wolves that would grow to eat five kilograms of meat per wolf per day at a time when food was very scarce. Starvation would have been a real threat to many carnivores in the Ice Age, and competition for food would have been fierce.^[97]:29 In 2002, a study highlighted that the ancestor of the dog appears more likely to have been a generalist canid and not the specialized modern gray wolf.^[62]

See further: Socialization - dogs and wolves

One dog behaviorist has stated that 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."^[97]:92

Prey pathway

The prey pathway was the way in which most major livestock species entered into domestication as these were once hunted by humans for their meat. Domestication was likely initiated when humans began to experiment with hunting strategies designed to increase the availability of these prey, perhaps as a response to localized pressure on the supply of the animal. Over time and with the more responsive species, these game-management strategies developed into herd-management strategies that included the sustained multi-generational control over the animals’ movement, feeding, and reproduction. As human interference in the life-cycles of prey animals intensified, the evolutionary pressures for a lack of aggression would have led to an acquisition of the same domestication syndrome traits found in the commensal domesticates.^[55][8][88]

Prey pathway animals include sheep, goats, cattle, water buffalo, yak, pig, reindeer, llama and alpaca. The right conditions for the domestication for some of them appear to have been in place in the central and eastern Fertile Crescent at the end of the Younger Dryas climatic downturn and the beginning of the Early Holocene about 11,700 YBP, and by 10,000 YBP people were preferentially killing young males of a variety of species and allowed the females to live in order to produce more offspring.^[55][8] By measuring the size, sex ratios, and mortality profiles of zooarchaeological specimens, archeologists have been able to document changes in the management strategies of hunted sheep, goats, pigs, and cows in the Fertile Crescent starting 11,700 YBP. A recent demographic and metrical study of cow and pig remains at Sha’ar Hagolan, Israel, demonstrated that both species were severely overhunted before domestication, suggesting that the intensive exploitation led to management strategies adopted throughout the region that ultimately led to the domestication of these populations following the prey pathway. This pattern of overhunting before domestication suggests that the prey pathway was as accidental and unintentional as the commensal pathway.^[8][88]

Directed pathway

The directed pathway was a more deliberate and directed process initiated by humans with the goal of domesticating a free-living animal. It probably only came into being once people were familiar with either commensal or prey-pathway domesticated animals. These animals were likely not to possess many of the behavioral preadaptions some species show before domestication. Therefore, the domestication of these animals requires more deliberate effort by humans to work around behaviors that do not assist domestication, with increased technological assistance needed.^[55][8][88]

Humans were already reliant on domestic plants and animals when they imagined the domestic versions of wild animals. Although horses, donkeys, and Old World camels were sometimes hunted as prey species, they were each deliberately brought into the human niche for sources of transport. Domestication was still a multi-generational adaptation to human selection pressures, including tameness, but without a suitable evolutionary response then domestication was not achieved.^[8] For example, despite the fact that hunters of the Near Eastern gazelle in the Epipaleolithic avoided culling reproductive females to promote population balance, neither gazelles^[76][8] nor zebras^[98][8] possessed the necessary prerequisites and were never domesticated. There is no clear evidence for the domestication of any herded prey animal originating in Africa.^[8]

Multiple pathways

The pathways that animals may have followed are not mutually exclusive. Pigs, for example, may have been domesticated as their populations became accustomed to the human niche, which would suggest a commensal pathway, or they may have been hunted and followed a prey pathway, or both.^[55][8][88]

Post-domestication gene flow

As agricultural societies migrated away from the domestication centers taking their domestic partners with them, they encountered populations of wild animals of the same or sister species. Because domestics often shared a recent common ancestor with the wild populations, they were capable of producing fertile offspring. Domestic populations were small relative to the surrounding wild populations, and repeated hybridizations between the two eventually led to the domestic population becoming more genetically divergent from its original domestic source population.^[99][87]

Advances in DNA sequencing technology allow the nuclear genome to be accessed and analyzed in a population genetics framework. The increased resolution of nuclear sequences has demonstrated that gene flow is common, not only between geographically diverse domestic populations of the same species but also between domestic populations and wild species that never gave rise to a domestic population.^[8] The yellow leg trait possessed by numerous modern commercial chicken breeds was acquired via introgression from the grey junglefowl indigenous to South Asia.^[100][8] African cattle are hybrids that possess both a European Taurine cattle maternal mitochondrial signal and an Asian Indicine cattle paternal Y-chromosome signature.^[101][8] Numerous other bovid species, including bison, yak, banteng, and gaur also hybridize with ease.^[102][8] Cats^[103][8] and horses^[104][8] have been shown to hybridize with many closely related species, and domestic honey bees have mated with so many different species they now possess genomes more variable than their original wild progenitors.^[105][8] The archaeological and genetic data suggests that long-term bidirectional gene flow between wild and domestic stocks - including donkeys, horses, New and Old World camelids, goats, sheep, and pigs - was common.^[89][8] Bidirectional gene flow between domestic and wild reindeer continues today.^[8]

The consequence of this introgression is that modern domestic populations can often appear to have much greater genomic affinity to wild populations that were never involved in the original domestication process. Therefore, it is proposed that the term "domestication" should be reserved solely for the initial process of domestication of a discrete population in time and space. Subsequent admixture between introduced domestic populations and local wild populations that were never domesticated should be referred to as "introgressive capture". Conflating these two processes muddles our understanding of the original process and can lead to an artificial inflation of the number of times domestication took place.^[87][8]

Some studies have found greater diversity in the genetic markers of dogs from East^[4][5] and Central^[6] Asia compared to Europe and have concluded that dogs originated from these regions, despite no archaeological evidence to support the conclusions.^[7] 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.^[7] Another reason is that none of the modern wolf populations are related to the Pleistocene wolves that were first domesticated.^[2] 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.^[8]

Refer: Admixture

Positive selection

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.^[14][106] 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.^{[78][107][87]} 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.^[108][87] Similar results for tameness and fear have been found for mink^[109] and Japanese quail.^[110] 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.^[87]

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.^[57][111][8] 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.^{[112][111][8]} 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.^[8]

Geneticists have identified more than 300 genetic loci and 150 genes associated with coat color variability.^[113][87] 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.^[114][87] Other studies have shown how human-induced selection is responsible for the allelic variation in pigs.^[115][87] 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.^[80][87]

In 2015, a study looked at over 100 pig genome sequences to ascertain their process of domestication. The process of domestication was assumed to have been initiated by humans, involved few individuals and relied on reproductive isolation between wild and domestic forms, but the study found that the assumption of reproductive isolation with population bottlenecks was not supported. The study indicated that pigs were domesticated separately in Western Asia and China, with Western Asian pigs introduced into Europe where they crossed with wild boar. 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.^[116][117]

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.^[118]

Unlike other domestic species which were primarily selected for production-related traits, dogs were initially selected for their behaviors.^[119][120] 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. These genes have been shown to have an impact on the catecholamine synthesis pathway, with the majority of the genes affecting the fight-or-flight response^[121][120] (i.e. selection for tameness), and emotional processing.^[120] Dogs generally show reduced fear and aggression compared to wolves. ^[122][120] 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.^[120]

See further: Dog learning by inference

Natural selection

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.^[97]: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.^{[97]:114[123]}

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.^[97]

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.^[97]: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.^[123]

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.^[124] 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.^[125]

Later studies support coevolution in that dogs can discriminate the emotional expressions of human faces,^[126] and that most people can tell from a bark whether a dog is alone, being approached by a stranger, playing, or being aggressive,^[127] and can tell from a growl how big the dog is.^[128]

Biological evidence

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.^[23][129]

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.^[130]

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.^[131] 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."^[132]:40

Lupification of humans

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?^[133]

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.^[134]

Marking of territory with signs such as pecked cupules, hand stencils and prints, abraded grooves, and finger impressions in once-soft mud are enduring signs used to mark occupation. They also became the first symbolic objects i.e. art. Wolves mark their territory with urine, but humans do not have the keen sense of smell as wolves and would have needed to use something more easily recognizable and enduring to mark their territory. Humans may have learned to mark their territory after watching wolves and dogs.^[134]

Hunting large animals in packs is a distinctive wolf behavioral trait. There is no evidence of big game hunting in pre-sapiens groups, but big-game hunting is very typical of homo sapiens that, in addition to climate change, may have contributed to the extinction of many large mammals. 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.^[134]

New forms of bonding might assist in living in large, complex and varied social groups. One of the keys to recent human survival has been the negotiation of situations by forming partnerships. Strong bonds exist between same-sex wolves, dogs and humans – bonds less fickle 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.^[134]

In 2003, a study compared the behavior and ethics of chimpanzees, wolves and humans. Humans' genetically closest relative appears to be a frightful caricature of human egoism, and even in their maternal behavior, warmth and affection are reduced to nursing and the occasional comforting hug. Cooperation among group members is limited to occasional hunting episodes or the persecution of a competitor, always aimed for one's own advantage. The closest approximation to human morality that can be found in nature is that of the gray wolf, Canis lupus. Wolves' 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 Cape hunting 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.^[133]

The mammoth steppe was the Eurasian tundra and grass steppe ecosystem which once stretched from Spain to the far east of Siberia, and at times continued into North America. On this steppe the wolves' ability to hunt in packs, to share risk fairly among pack members, and to cooperate moved them to the top of the food pyramid above lions, hyenas and bears. Some, but not all, 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 ice age, some of our ancestors teamed up with those pastoralist wolves. 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. These pastoralists later became herders. From a biologist's vantage point, the interwining process of hominization and canization makes sense only if viewed in terms of coevolution.^[133]

References

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