Origin of the domestic dog

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.^[55] 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 another 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.^[56] The ancestors of modern humans first reached Europe between 43,000-45,000 years BP, with their remains found in Italy^[57] and in Britain.^[58]

See further: Paleoecology at this time

Probable ancestor

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.

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 led 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.^[15] Some researchers propose that the "dog was the dog before it was domesticated"^[59] and that the ancestor of Canis familiaris was a wild Canis familiaris,^[60] which had diverged from a common ancestor along with the gray wolf.^[61]

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.^[7] Two later studies using whole genome sequencing indicated divergence times of 32,000 YBP^[62] or 11,000-16,000 YBP,^[8] with the assumed mutation rate "the dominant source of uncertainty in dating the origin of dogs."^[8]

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. 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.^[41] 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.^[41][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.^[41] The study proposed that the timing of this separation of the dog and wolf did not have to coincide with selective breeding by humans.^{[15][41]:3[63]}

In 2017, a study compared the nuclear genome sequences of Neolithic dog specimens with sequences from over 5,000 dogs and wolves. These Neolithic dog specimens included a dog sample from the Early Neolithic site in Herxheim, Germany dated 7,000 YBP, one from the Late Neolithic site of Kirschbaum (Cherry Tree) Cave near Forchheim, Germany dated 4,700 YBP, and one found in the Late Neolithic passage grave at Newgrange, Ireland dated 4,800 YBP. The study calculated a mutation rate for the 7,000 YBP Neolithic dog and found that it matched the mutation rate of the Taimyr-1 specimen, and noted that this also matched the mutation rate for the Newgrange dog that had been calculated in an earlier study. Using the 7,000 YBP specimen and this mutation rate, the dog-wolf divergence time is estimated to have occurred 36,900-41,500 YBP and this is consistent with the timing found with the Taimyr-1 specimen in an earlier study.^[51]

In 2018, a study looked at the y-chromosome male lineage of canines, including the ancient fossils of the Herxheim, Kirschbaum, and Newgrange dogs. The study identified six major dog yDNA haplogroups, of which two of these include the majority of modern dogs. The Newgrange dog fell into the most commonly occurring of these haplogroups. The two ancient German dogs fell into a haplogroup commonly found among dogs from the Middle East and Asia, with the Kirschbaum dog sharing a common male lineage with the extant Indian wolf. The study concluded that at least 2 different male haplogroups existed in ancient Europe, and that the dog male lineage diverged from its nearest common ancestor shared with the gray wolf sometime between 68,000-151,000 YBP.^[40]

Using modern DNA

Europe In 2007, a study of maternal mDNA sequences from dogs and wolves indicated that their haplotypes resolved into four monophyletic clades (a grouping that includes its ancestor), of which two clades showed a strong relationship between dogs and the wolves of Europe.^[7][52]

South East Asia: In 2009, a study of the maternal mitochondrial genome indicated the origin in south-eastern Asia south of the Yangtze River as more dog haplogroups had been found there.^[71] 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.^[72] 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.^[12]

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.^[6] In 2011, a study found that there had been dog-wolf hybridization and not an independent domestication.^[8][73]

East Asia: In 2002, a study of maternal mDNA indicated 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,^[74] but this was rebutted because village dogs in Africa also show a similar haplotype diversity.^[75] 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.^[17] 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.^[12]

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.^[16]

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,^[6] genome-wide similarities with Chinese wolves,^[17] and lower linkage disequilibrium^[16] might reflect regional admixture between dogs with wolves and gene flow between dog populations, with genetically 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.^[2]

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^[3] (courtesy Hannes Napierala)

In his 1868 book on Variation under Domestication, Charles Darwin assessed the arguments for single or multiple origins of dogs, and noted the paleontological research of de Blainville who proposed that dogs were descended from a single extinct species.^[76] In 1934, an eminent paleontologist indicated that the ancestor of the dog lineage may have been the extinct Canis variabilis.^[38] In 1950, a morphological study of Japanese prehistoric dogs compared to extant wolves concluded: "Therefore the living wolf kinds have nothing to do with the ancestral forms of the prehistoric dog races."^[77] 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.^[49] 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.^[12]

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.^[3][7][78] 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 Kessleroch cave near Thayngen in the canton of Schaffhausen, 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 another 14,500 YBP wolf sequence also from the Kesserloch cave, 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.^[48][3] The data supports the hypothesis that dog domestication preceded the emergence of agriculture^[7] and was initiated close to the Last Glacial Maximum when hunter-gatherers preyed on megafauna.^[3][79]

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^[3] as there was for domestic pigs.^[80]

One theory is that domestication occurred during one of the five cold Heinrich events that occurred after the arrival of humans in West Europe 37 000, 29 000, 23 000, 16 500 and 12 000 YBP. The theory is that the extreme cold during one of these events caused humans to either shift their location, adapt through a breakdown in their culture and change of their beliefs, or adopt innovative approaches. The adoption of the large wolf/dog was an adaptation to this hostile environment.^[81]

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.^[17] 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.^[12]

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.^[82]

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.^[82]

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".^[11]

Later studies suggested that it was possible for multiple primitive forms of the dog to have existed, including in Europe.^[17] European dog populations had undergone extensive turnover during the last 15,000 years that has erased the genomic signature of early European dogs,^[16][83] the genetic heritage of the modern breeds has become blurred due to admixture,^[12] and there was the possibility of past domestication events that had gone extinct or had been largely replaced by more modern dog populations.^[16]

In 2016, a study compared the mitochondrial DNA and whole-genome sequences of a worldwide 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 not as able 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.^[18] As the taxonomic classification of the "proto-dog" Paleolithic dogs as being either dogs or wolves remains controversial, they were excluded from the study.^[18]: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.^[80] (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.^[18][84] Two domestication events in Western Eurasia and Eastern Eurasia has recently been found for the domestic pig.^[18][80]

The hypothesis is that two genetically different, and possibly now extinct, wolf populations were domesticated independently in eastern and western Eurasia to produce paleolithic dogs.^[18] The eastern Eurasian dogs then dispersed westward alongside humans, reaching western Europe 6,400–14,000 years ago where they partially replaced the western paleolithic dogs.^[48][18] 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.^[85]

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.^[18] Immediately after divergence, the dog population outnumbered the wolf population, and later the dog population underwent a population reduction to be much lower than that of the wolf.^{[18]:Fig2[86]}

Neolithic dogs – one domestication event

In 2017, a study compared the nuclear genome sequences of three Neolithic dog specimens from Germany and Ireland with sequences from over 5,000 dogs and wolves. The study found that modern European dogs descended from their Neolithic ancestors with no evidence of a population turnover found by an earlier study. The study found that a single dog-wolf divergence occurred 36,900-41,500 YBP, followed by a divergence between Southeast Asian and Western Eurasian dogs 17,500-23,900 YBP and this indicates a single dog domestication event occurring between 20,000-40,000 YBP. The study did not support a dual domestication event found by an earlier study.^[51]

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][7][78] Other studies that included a wider sample of specimens have reported two rare East Asian clades E-F with weaker statistical support.^[71][74][95] 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.^[71][95]

Haplogroup A: Includes 64-65% of dogs.^[3][95] Haplotypes of subclades a2–a6 are derived from post-domestication wolf–dog hybridization.^[71][95]

Haplogroup B: Includes 22-23% of dogs.^[3][95] haplotypes of subclade b2 are derived from post-domestication wolf–dog hybridization.^[71][95]

Haplogroup C: Includes 10-12% of dogs.^[3][95]

Haplogroup D: Derived from post-domestication wolf–dog hybridization in subclade d1 (Scandinavia) and d2 (South-West Asia).^[71][95] 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^[113] 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.^[73]

Haplogroup E: Derived from post-domestication wolf–dog hybridization in East Asia,^[71][95] (rare distribution in South-East Asia, Korea and Japan).^[73]

Haplogroup F: Derived from post-domestication wolf–dog hybridization in Japan.^[71][95] A study of 600 dog specimens found only one dog whose sequence indicated hybridization with the extinct Japanese wolf.^[114]

It is not known whether this hybridization was the result of humans selecting for phenotypic traits from local wolf populations^[78] or the result of natural introgression as the dog expanded across Eurasia.^[12]

In 2018, a study found a small amount of dog ancestry in 62% of Eurasian wolf specimens looked at, that hybridization had occurred across a wide number of timescales and not just recently, however in contrast there was almost no admixture detected in the North American specimens. There was introgression of the male dog into the wolf, but also one hybrid detected which was the result of a male wolf crossed with a female dog. Wolves have maintained their phenotype differences from the dog, which indicates low-frequency hybridization. The conclusion is that phenotype is no indication of "purity" and the definition of pure wolves is ambiguous. Free-ranging dogs across Eurasia show introgression from wolves.^[115] Another study found that the β-defensin gene responsible for the black coat of North American wolves was the result of a single introgression from dogs in the Yukon dated between 1,600-7,200 years ago. The study proposes that early Native American dogs were the source.^[116]

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

Taimyr wolf admixture

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.^[41]: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.^[41]:3–4

An attempt to explore admixture between Taimyr-1 and gray wolves produced unreliable results.^[41]: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.^[15]

Behavior

Unlike other domestic species which were primarily selected for production-related traits, dogs were initially selected for their behaviors.^[130][131] 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^[131][132] 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.^[131] Dogs generally show reduced fear and aggression compared to wolves.^[131][133] 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.^[131]

In 2018, a study identified 429 genes that differed between modern dogs and modern wolves. As the differences in these genes could also be found in ancient dog fossils, these were regarded as being the result of the initial domestication and not from recent breed formation. These genes are linked to neural crest and central nervous system development. These genes affect embryogenesis and can confer tameness, smaller jaws, floppy ears, and diminished craniofacial development, which distinguish domesticated dogs from wolves and are considered to reflect domestication syndrome. The study proposes that domestication syndrome is caused by alterations in the migration or activity of neural crest cells during their development. The study concluded that during early dog domestication, the initial selection was for behavior. This trait is influenced by those genes which act in the neural crest, which led to the phenotypes observed in modern dogs.^[134]

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.^[8][131] 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.^[8] 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.^[135]

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.^[136] Prey capture rates may have increased in comparison to wolves and with it the amount of lipid consumed by the assisting proto-dogs.^{[136][79][137]} 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.^[136] 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.^[138]

See further: Phenotypic plasticity

Biological evidence

Montage showing the coat variation of the dog.

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.^[143][144]

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.^[62][145]

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.^[146] Like the Tibetan people, Tibetan mastiffs appear to have derived these benefits partially from the EPAS1 gene, acquired through introgression.^[147]

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.^[148] 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."^[21]

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.^[139]: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.^[140]

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.^[149] 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.^[150]

Later studies support coevolution in that dogs can discriminate the emotional expressions of human faces,^[151] and that most people can tell from a bark whether a dog is alone, being approached by a stranger, playing, or being aggressive,^[152] and can tell from a growl how big the dog is.^[153]

Human adoption of some wolf behaviors

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.^[154] 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.^[154][155] 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.^[154] One of the keys to recent human survival has been the forming of 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.^[154][156]

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.^[100][157] 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,^[100][101] 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.^[100] Social sharing within families may be a trait that early humans learned from wolves,^[100][158] and with wolves digging dens long before humans constructed huts it is not clear who domesticated whom.^{[52][100][157]}

Bison surrounded by gray wolf pack

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.^[52] 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 study proposed that during the Last Glacial Maximum, some of our ancestors teamed up with those pastoralist wolves and learned their techniques.^[100][159] 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.^[52][100]