The dog diverged from a now-extinct population of wolves immediately before the Last Glacial Maximum, when much of Eurasia was a cold, dry mammoth steppe biome.
The origin of the domestic dog is not clear. The domestic dog is a member of the genus Canis, which forms part of the wolf-like canids, and is the most widely abundant terrestrial carnivore. The closest living relative of the dog is the extant gray wolf, and there is no evidence of any other canine contributing to its genetic lineage. The dog and the extant gray wolf are sister taxa, as modern wolves are not closely related to the wolves that were first domesticated. The archaeological record and genetic analysis show the remains of the Bonn–Oberkassel dog buried beside humans 14,200 years ago to be the first undisputed dog, with disputed remains occurring 36,000 years ago. These dates imply that the earliest dogs arose in the time of human hunter-gatherers and not agriculturists. The dog was the first species to be domesticated.
Where the genetic divergence of dog and wolf took place remains controversial, with the most plausible proposals spanning Western Europe,[3][15] Central Asia[15][16] and East Asia.[15][17] This has been made more complicated by the most recent proposal that fits the available evidence, which is that an initial wolf population split into East and West Eurasian groups; these, before going extinct, were domesticated independently into two distinct dog populations between 14,000 and 6,400 years ago. The Western Eurasian dog population was partially and gradually replaced by East Asian dogs introduced by humans at least 6,400 years ago.
Canid and human evolution
Six million years ago, towards the close of the Miocene era, the earth's climate was gradually cooling and this led to the glaciations of the Pliocene and the Pleistocene – the Ice Age. In many areas, forests and savannahs were replaced with steppe or grasslands and only those creatures that could adapt survived.In southern North America, small woodland foxes grew bigger and better adapted to running, and by the late Miocene the first of the genus Canis had arisen - the ancestors of coyotes, wolves and the domestic dog. In eastern Africa, a split occurred among the large primates. Some remained in the trees, while others came down from the trees, learned to walk upright, developed larger brains, and in the more open country learned to avoid predators while becoming predators themselves.[20] The two species ultimately met in Eurasia.
"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." — Mark Derr[21]Human hunter-gathers did not live in fear of nature and knew that they posed a formidable risk to any potential predators. The Ju'wasi people of Namibia share their land with prides of lions. Both species coexist with respect and without fear or hostility in a relationship that may go back to the dawn of modern humans. The lion is a larger and far more dangerous predator than the wolf. Early modern humans entering Eurasia and first encountering packs of wolves may have been assisted in living among them because of the traditional beliefs of their African ancestors. In historical times, mutual respect and cooperation with canids can be found in the stories and traditions of the indigenous peoples of Siberia, East Asia, North America, and Australia.[22]
Dog evolution
Evolution (from the Latin evolutio: "unrolling")[23] is defined by the English naturalist, geologist and biologist Charles Darwin as biological descent with modification.[24] Evolution eventually splits ancestral populations into new species which cannot, or will not, interbreed.[25]The domestic dog is the first species and the only large carnivore to have been domesticated. Over the past 200 years, dogs have undergone rapid phenotypic change and were formed into today's modern dog breeds due to artificial selection imposed by humans. These breeds can vary in size and weight from a 0.46 kg (1.0 lb) teacup poodle to a 90 kg (200 lb) giant mastiff. The skull, body, and limb proportions vary significantly between breeds, with dogs displaying more phenotypic diversity than can be found within the entire order of carnivores. Some breeds demonstrate outstanding skills in herding, retrieving, scent detection, and guarding, which demonstrates the functional and behavioral diversity of dogs. There have been major advances in understanding the genes that gave rise to the phenotypic traits of dogs. The first dogs were certainly wolflike, however the phenotypic changes that coincided with the dog–wolf genetic divergence are not known.[26]
The causes and context of dog domestication are not known. Deriving a time and a place for domestication could help describe the conditions that gave rise to an association of a large carnivore with hunter-gatherers. All other domestication events occurred during or after the development of agriculture, which was approximately 10,000 years before present (YBP). The earlier association of dogs with humans may have allowed dogs to have a profound influence on the course of early human history and the development of civilization. However, the timing, geographic locations, and ecological conditions that led to dog domestication are not agreed.[26]
Genetic studies indicate that the gray wolf is the closest living relative of the dog, with no evidence of any other canine species having contributed. Attempting to reconstruct the dog's lineage through the phylogenetic analysis of DNA sequences from modern dogs and wolves has given conflicting results for several reasons. Firstly, studies indicate that an extinct Late Pleistocene wolf is the nearest common ancestor to the dog, with modern wolves not being the dog's direct ancestor. Secondly, the genetic divergence between the dog and modern wolves occurred over a short period of time, so that the time of the divergence is difficult to date (referred to as incomplete lineage sorting). This is complicated further by the cross-breeding that has occurred between dogs and wolves since domestication (referred to as post-domestication gene flow). Finally, there has been only tens of thousands of generations of dogs since domestication, so that the number of mutations between the dog and the wolf are few and this makes the timing of domestication difficult to date.[26]
Archaeological evidence
| The Upper Paleolithic |
|
|---|---|
Upper Paleolithic (40–10 ka)
|
The debate centres around Homo sapiens and if they had entered into cooperation with wolves soon after they moved into Eurasia, and if so when and where did these wolves change into domesticated dogs. In arguing that domestication leads to reduction in size, the late domestication theory ignores that modern horses and pigs are larger than their wild ancestors. It also ignores that if hunter-gathers entered into a hunting relationship with wolves then there would be no need of selection for a reduction in size. A reduction in size would have occurred much later when humans moved into agricultural villages. The late domestication theory does not consider the possibility that humans may have formed a relationship with non-domesticated wolves and that dogs in the early stages of domestication might be indistinguishable from wolves. According to indigenous North Americans, over the past 20,000 years the canids living with them were wolves that could not be distinguished as dogs.[27]
The problem in attempting to identify when and where domestication occurred is the possibility that the process of domestication occurred in a number of places and at a number of times throughout prehistory.[27] Early dog remains have been found in different parts of the world. This suggests that dog domestication may have taken place in different regions independently by hunter-gatherers, in some cases at the same time[35] and in other cases at different times,[36] with different wolf subspecies producing different dog lineages.[37][36] Therefore, the number of dog domestication events is not known.[38] A maternal mDNA study shows that dogs fall within 4 clades,[3] indicating that dogs are derived from 4 separate lineages and that there was no single domestication event.[27]
A 2018 domestication study looked at the reasons why the archeological record that is based on the dating of fossil remains often differed from the genetic record contained within the cells of living species. The study concluded that our inability to date domestication is because domestication is a continuum and there is no single point where we can say that a species was clearly domesticated using these two techniques. The study proposes that changes in morphology across time and how humans were interacting with the species in the past needs to be considered in addition to these two techniques.[39]
..."wild" and "domesticated" exist as concepts along a continuum, and the boundary between them is often blurred — and, at least in the case of wolves, it was never clear to begin with. — Raymond Pierotti[22]The table below lists by location and timing in years before present the very early co-location of hominid and wolf specimens, followed by proposed Paleolithic dogs and then the first undisputed dog remains.
| Years BP | Location | Finding |
|---|---|---|
| 400,000 | Boxgrove near Kent, England | Wolf bones in close association with hominid bones. These have been found in Lower Paleolithic sites including Boxgrove (400,000 YBP), Zhoukoudian in North China (300,000 YBP), and Grotte du Lazaret (125,000 YBP) in southern France. "The sites of occupation and hunting activities of humans and wolves must often have overlapped."[40] We do not know if the co-location was the result of coincidence or a relationship. |
| 300,000 | Zhoukoudian cave system, China | Small, extinct wolf skulls of Canis variabilis. At the site, the small wolf's remains were in close proximity to Peking man (Homo erectus pekinensis).[41] We do not know if the co-location was the result of coincidence or a relationship. |
| 125,000 | Grotte du Lazaret, near Nice, France | Wolf skulls appear to have been set at the entrance of each dwelling in a complex of Paleolithic shelters. The excavators speculated that wolves were already incorporated into some aspect of human culture by this early time. A nearby wolf den intruded on the site.[42] In 1997, a study of maternal mDNA indicated that the genetic divergence of dogs from wolves occurred 100,000–135,000 YBP.[7] The Lazaret excavation lends credence to this mDNA study, in addition to indicating that a special relationship existed between wolves and genus Homo other than Homo sapiens, because this date is well before the arrival of Homo sapiens into Europe.[27] In 2018, a study of paternal yDNA indicated that the dog and the modern gray wolf genetically diverged from a common ancestor between 68,000-151,000 YBP.[43] |
| 36,000 – 32,000[27] | Goyet Cave, Samson River Valley, Belgium | The "Goyet dog" is proposed as being a Paleolithic dog.[11] The dog-like skull was found in a side gallery of the cave, and Palaeolithic artifacts in this system of caves date from the Mousterian, Aurignacian, Gravettian, and Magdalenian, which indicates recurrent occupations of the cave from the Pleniglacial until the Late Glacial.[11] The Goyet dog left no descendants, and its genetic classification is inconclusive because its mitochondrial DNA (mDNA) does not match any living wolf nor dog. It may represent an aborted domestication event or phenotypically and genetically distinct wolves.[3] A genome-wide study of a 35,000 YBP Pleistocene wolf fossil from northern Siberia indicates that the dog and the modern grey wolf genetically diverged from a common ancestor between 27,000-40,000 YBP.[44][27] |
| 33,500 | Razboinichya Cave, Altai Mountains, Central Asia (Russia) | The "Altai dog" is proposed as being a Paleolithic dog.[11] The specimens discovered were a dog-like skull, mandibles (both sides) and teeth. The morphological classification, and an initial mDNA analysis, found it to be a dog.[45] A later study of its mDNA was inconclusive, with 2 analyses indicating dog and another 2 indicating wolf. In 2017, two prominent evolutionary biologists reviewed the evidence and supported the Altai dog as being a dog from a lineage that is now extinct and that was derived from a population of small wolves that are also now extinct.[26] |
| 32,000–13,500 | Europe and Yakutia, northeastern Siberia | Numerous Paleolithic dog remains found in Europe and one in Yakutia, northeast Siberia. |
| 14,200 | Bonn-Oberkassel, Germany | The "Bonn-Oberkassel dog". Undisputed dog skeleton buried with a man and woman. All three skeletal remains were found sprayed with red hematite powder.[10] The consensus is that a dog was buried along with two humans.[46] Analysis of mDNA indicates that this dog was a direct ancestor of modern dogs.[47] |
Genetics, archaeology and morphology
The domestic dog is the most widely abundant large carnivore. When and where dogs were first domesticated has taxed geneticists for the past 20 years and archaeologists for many decades longer.[9] 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.[12]However, recent studies based on genetics propose five generalizations about dogs.[49]
- Over the past million years, numerous wolf-like forms existed but their turnover has been high, and modern wolves are not the lineal ancestors of dogs.[2][3][8][50] Although research had suggested that dogs and wolves were genetically very close relatives,[51][7][52][53] later phylogenetic analysis strongly supported the hypothesis that the dog forms a monophyletic clade that is sister to Eurasian wolves, and these together form a sister clade to North American wolves.[2][49] This indicates that an extant wolf population ancestral to dogs has not been found, and is presumed that the wolves immediately ancestral to dogs are extinct.[8][9][51] The dog is not a separate species to the wolf.[2][49]
- Studies propose a divergence time of the dog from the wolf ancestor closer to 27,000 YBP,[2][3][8][18][44] with the most recent proposing 36,900-41,500 YBP followed by domestication occurring between 20,000-40,000 YBP.[54]
- The dog was the first domesticated species[9][12][13][14] and appeared more than 15,000 years before present (YBP). The dog was established across Eurasia before the end of the Late Pleistocene era, well before cultivation and the domestication of other animals around 10,000 YBP,[12] indicating that dogs were domesticated by hunter-gatherers and not early agriculturalists.[55] Studies support two population bottlenecks had occurred to the dog lineage, one due to the initial domestication and one due to the formation of dog breeds.[49]
- Dogs show both ancient and modern lineages. The ancient lineages appear most in Asia but least in Europe because the Victorian era development of modern dog breeds used little of the ancient lineages.[6][16][18] All dog populations (breed, village, and feral) show some evidence of genetic admixture between modern and ancient dogs. Some ancient dog populations that once occupied Europe and the New World no longer exist.[3][9][18][56] This implies that some ancient dog populations were entirely replaced and others admixed over a long period of time.[49]
- There was admixture between dog and regional wolf populations except on the Tibetan Plateau and in the New World wolves.[2][8] This admixture has occurred throughout history and as dogs expanded across the landscape. There are some dog populations that show recent admixture with wolves.[2][49]
Time of divergence
Paleoecology
Mammoth bone dwelling, Mezhirich site, Ukraine
During the last Ice Age, the most recent peak is known as the Last Glacial Maximum when a vast mammoth steppe stretched from Spain eastwards across Eurasia and over the Bering land bridge into Alaska and the Yukon. The continent of Europe was much colder and drier than it is today, with polar desert in the north and the remainder steppe or tundra. Forest and woodland were almost non-existent except for isolated pockets in the mountain ranges of southern Europe.[58] 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.[59] The ancestors of modern humans first reached Europe between 43,000-45,000 years BP, with their remains found in Italy[60] and in Britain.[61]
Probable ancestor
_Wolf.png)
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.
Evolutionary divergence
.jpg)
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"[62] and that the ancestor of Canis familiaris was a wild Canis familiaris,[63] which had diverged from a common ancestor along with the gray wolf.[64]
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[65] or 11,000-16,000 YBP,[8] with the assumed mutation rate "the dominant source of uncertainty in dating the origin of dogs."[8]
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.[44] 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.[44][27] 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.[44] The study proposed that the timing of this separation of the dog and wolf did not have to coincide with selective breeding by humans.
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.[54]
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.[43]
Place of divergence
Where the genetic divergence of dog and wolf took place remains controversial, with the most plausible proposals spanning Western Europe,[3][15] Central Asia,[15][16] and East Asia.[15][17] This has been made more complicated by the most recent proposal that fits the available evidence, which is that an initial wolf population split into East and West Eurasian wolves, these were then domesticated independently before going extinct into two distinct dog populations between 14,000-6,400 years ago, and then the Western Eurasian dog population was partially and gradually replaced by East Asian dogs that were brought by humans at least 6,400 years ago.[15][18][19]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][55]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.[67] 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.[68] 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][69]
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,[70] but this was rebutted because village dogs in Africa also show a similar haplotype diversity.[71] 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.[72] In 1934, an eminent paleontologist indicated that the ancestor of the dog lineage may have been the extinct Canis variabilis.[41] 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."[73] 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.[52] 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][74] 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.[51][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][75]
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.[76]
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.[77]
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.[78]
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.[78]
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][79] 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.
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][80] Two domestication events in Western Eurasia and Eastern Eurasia has recently been found for the domestic pig.[18][76]
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.[51][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.[81]
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]
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.[54]Dog domestication
The domestication of animals is the scientific theory of the mutual relationship between animals with the humans who have influence on their care and reproduction.[84] 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.[72][85][86]There is a genetic difference between domestic and wild populations. There is also such a difference between the domestication traits that researchers believe to have been essential at the early stages of domestication, and the improvement traits that have appeared since the split between wild and domestic populations.[9][87][88] Domestication traits are generally fixed within all domesticates, and were selected during the initial episode of domestication of that animal or plant, whereas improvement traits are present only in a proportion of domesticates, though they may be fixed in individual breeds or regional populations.[9][88][89] The dog was the first domesticant and was established across Eurasia before the end of the Late Pleistocene era, well before cultivation and before the domestication of other animals.[12]
Time of domestication
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.
An apex predator is a predator that sits on the top trophic level of the food chain, while a mesopredator sits further down the food chain and is dependent on smaller animals. Towards the end of the Pleistocene era, most of today's apex predators were mesopredators and this included the wolf. During the ecological upheaval associated with the close of the Late Pleistocene, one type of wolf population rose to become today's apex predator and another joined with humans to become an apex consumer.[57]
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).[90]
Socialization
Humans and wolves both exist in complex social groups. How humans and wolves got together remains unknown. One view holds that domestication as a process that is difficult to define. The term was developed by anthropologists with a human-centric view in which humans took wild animals (ungulates) and bred them to be "domestic", usually in order to provide improved food or materials for human consumption. That term may not be appropriate for a large carnivore such as the dog. This alternate view regards dogs as being either socialized and able to live among humans, or unsocialized. There exists today dogs that live with their human families but are unsocialized and will threaten strangers defensively and aggressively no different from a wild wolf. There also exists a number of cases where wild wolves have approached people in remote places, attempting to initiate play and to form companionship.[91] One such notable wolf was Romeo, a gentle black wolf that formed relationships with the people and dogs of Juneau, Alaska.[92] This view holds that before there could have been domestication of the wolf, there had to have been its socialization.[91][93]Commensal pathway
Montage showing the morphological variation of the dog.
Animal domestication is a coevolutionary process in which a population responds to selective pressure while adapting to a novel niche that included another species with evolving behaviors.[9]
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.[12] It may have been inevitable that the first domesticated animal came from the order of carnivores as these are less afraid when approaching other species. Within the carnivores, the first domesticated animal would need to exist without an all-meat diet, possess a running and hunting ability to provide its own food, and be of a controllable size to coexist with humans, indicating the family Canidae, and the right temperament[94]:p166 with wolves being among the most gregarious and cooperative animals on the planet.[95][96]
Ancient DNA supports the hypothesis that dog domestication preceded the emergence of agriculture[3][7] 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] Wolves were probably attracted to human campfires by the smell of meat being cooked and discarded refuse in the vicinity, first loosely attaching themselves and then considering these as part of their home territory where their warning growls would alert humans to the approach of outsiders.[97] 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.[98] The earliest sign of domestication in dogs was the neotonization of skull morphology[98][99][100] and the shortening of snout length that results in tooth crowding, reduction in tooth size, and a reduction in the number of teeth,[101][98] which has been attributed to the strong selection for reduced aggression.[98][99] This process may have begun during the initial commensal stage of dog domestication, even before humans began to be active partners in the process.[9][98]
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.[9][102] A study has identified the remains of a population of extinct Pleistocene Beringian wolves with unique mitochondrial signatures. The skull shape, tooth wear, and isotopic signatures suggested these were specialist megafauna hunters and scavengers that became extinct while less specialized wolf ecotypes survived.[9][103] 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.[9][104]
Even today, the wolves on Ellesmere Island do not fear humans, which is thought to be due to them seeing humans so little, and they will approach humans cautiously, curiously and closely.
Post-domestication gene flow
Some studies have found greater diversity in the genetic markers of dogs from East[17][67] and Central[16] Asia compared to Europe and have concluded that dogs originated from these regions, despite no archaeological evidence to support the conclusions.[12] 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.[12] Another reason is that none of the modern wolf populations are related to the Pleistocene wolves that were first domesticated.[8] 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.[9]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][74] Other studies that included a wider sample of specimens have reported two rare East Asian clades E-F with weaker statistical support.[67][70][90] 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.[67][90]Haplogroup A: Includes 64-65% of dogs.[3][90] Haplotypes of subclades a2–a6 are derived from post-domestication wolf–dog hybridization.[67][90]
Haplogroup B: Includes 22-23% of dogs.[3][90] haplotypes of subclade b2 are derived from post-domestication wolf–dog hybridization.[67][90]
Haplogroup C: Includes 10-12% of dogs.[3][90]
Haplogroup D: Derived from post-domestication wolf–dog hybridization in subclade d1 (Scandinavia) and d2 (South-West Asia).[67][90] 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[109] 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.[69]
Haplogroup E: Derived from post-domestication wolf–dog hybridization in East Asia,[67][90] (rare distribution in South-East Asia, Korea and Japan).[69]
Haplogroup F: Derived from post-domestication wolf–dog hybridization in Japan.[67][90] A study of 600 dog specimens found only one dog whose sequence indicated hybridization with the extinct Japanese wolf.[110]
It is not known whether this hybridization was the result of humans selecting for phenotypic traits from local wolf populations[74] 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.[111] 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.[112]
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.[44]: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.[44]:3–4
An attempt to explore admixture between Taimyr-1 and gray wolves produced unreliable results.[44]: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]
Positive selection
Reduction in size under domestication - grey wolf and chihuahua skulls.
The wolf's family portrait reveals a diversity of form among breeds of domestic dogs.
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.[72][86] 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 Dmitry Belyayev 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.[99][113][114] 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.[113][115] Similar results for tameness and fear have been found for mink[116] and Japanese quail.[117] 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.[113]
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.[9][87][88] 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.[9][88][89] 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.[9] A study published in 2016 suggested that there have been negative genetic consequences of the domestication process as well, that enrichment of disease-related gene variants accompanied positively selected traits.[118]
In 2010, a study identified 51 regions of the dog genome that were associated with phenotypic variation among breeds in 57 traits studied, which included body, cranial, dental, and long bone shape and size. There were 3 quantitative trait loci that explained most of the phenotypic variation. Indicators of recent selection were shown by many of the 51 genomic regions that were associated with traits that define a breed, which include body size, coat characteristics, and ear floppiness.[119] Geneticists have identified more than 300 genetic loci and 150 genes associated with coat color variability.[113][120] 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.[113][121] Other studies have shown how human-induced selection is responsible for the allelic variation in pigs.[113][122] 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.[113][123]
In 2015, a study looked at over 100 pig genome sequences to ascertain their process of domestication. A model that fitted the data included admixture with a now extinct ghost population of wild pigs during the Pleistocene. The study also found that despite back-crossing with wild pigs, the genomes of domestic pigs have strong signatures of selection at genetic loci that affect behavior and morphology. The study concluded that human selection for domestic traits likely counteracted the homogenizing effect of gene flow from wild boars and created domestication islands in the genome. The same process may also apply to other domesticated animals.[76][124]
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.[125]
Behavior
Unlike other domestic species which were primarily selected for production-related traits, dogs were initially selected for their behaviors.[126][127] 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[127][128] 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.[127] Dogs generally show reduced fear and aggression compared to wolves.[127][129] 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.[127]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][127] 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.[130]
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.[131] Prey capture rates may have increased in comparison to wolves and with it the amount of lipid consumed by the assisting proto-dogs.[131][75][132] 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.[131] 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.[133]
Natural selection
Dogs can infer the name of an object and have been shown to learn the names of over 1,000 objects. Dogs can follow the human pointing gesture; even nine-week-old puppies can follow a basic human pointing gesture without being taught. New Guinea singing dogs, a half-wild proto-dog endemic to the remote alpine regions of New Guinea, as well as dingoes in the remote Outback of Australia are also capable of this. These examples demonstrate an ability to read human gestures that arose early in domestication and did not require human selection. "Humans did not develop dogs, we only fine-tuned them down the road."[134]:92A 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.[134]: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.[134]:114[135] The more docile animals have been found to have less testosterone than their more aggressive counterparts, and testosterone controls aggression and brain size. One researcher has argued that in becoming more social, we humans have developed a smaller brain than those of humans 20,000 years ago.[136]
Dog and human convergent evolution
As a result of the domestication process there is also evidence of convergent evolution having occurred between dogs and humans.[134] The history of the two is forever intertwined.[137]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.[138][139]
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.[65][140]
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.[141] Like the Tibetan people, Tibetan mastiffs appear to have derived these benefits partially from the EPAS1 gene, acquired through introgression.[142]
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.[143] 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.[134]: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.[135]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.[144] 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.[145]
Later studies support coevolution in that dogs can discriminate the emotional expressions of human faces,[146] and that most people can tell from a bark whether a dog is alone, being approached by a stranger, playing, or being aggressive,[147] and can tell from a growl how big the dog is.[148]
Human adoption of some wolf behaviors
| “ | ... Isn't it strange that, our being such an intelligent primate, we didn't domesticate chimpanzees as companions instead? Why did we choose wolves even though they are strong enough to maim or kill us? ... | ” |
| — Wolfgang Schleidt[95] | ||
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.[95][152] 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,[95][96] 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.[95] Social sharing within families may be a trait that early humans learned from wolves,[95][153] and with wolves digging dens long before humans constructed huts it is not clear who domesticated whom.[55][95][152]
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.[55] 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.[95][154] 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.[55][95]
First dogs
Bonn–Oberkassel dog
In 1914, on the eve of the First World War, two human skeletons were discovered during basalt quarrying at Oberkassel, Bonn in Germany. With them were found a right mandible of a "wolf" and other animal bones.[155] After the end of the First World War, in 1919 a full study was made of these remains. The mandible was recorded as "Canis lupus, the wolf" and some of the other animal bones were assigned to it.[156] The remains were then stored and forgotten for fifty years. In the late 1970s there was renewed interest in the Oberkassel remains and the mandible was re-examined and reclassified as belonging to a domesticated dog.[157][158][159] The mitochondrial DNA sequence of the mandible was matched to Canis lupus familiaris - dog,[3] and confirms that the Oberkassel dog is a direct ancestor of today’s dogs.[47] The bodies were dated to 14,223 YBP.[10] This implies that in Western Europe there were morphologically and genetically "modern" dogs in existence around 14,500 years ago.[46]Later studies assigned more of the other animal bones to the dog until most of a skeleton could be assembled.[46] The humans were a man aged 40 years and a woman aged 25 years. All three skeletal remains were found covered with large 20 cm thick basalt blocks and were sprayed with red hematite powder.[10] The consensus is that a dog was buried along with two humans.[46] A tooth belonging to a smaller and older dog was also identified but it had not been sprayed with red powder.[10] The cause of the death of the two humans is not known.[46] A pathology study of the dog remains suggests that it had died young after suffering from canine distemper between ages 19 and 23 weeks.[10] The dog could not have survived during this period without intensive human care.[46][10] During this period the dog was of no utilitarian use to humans,[10] and suggests the existence of emotional or symbolic ties between these humans and this dog.[46] In conclusion, near the end of the Late Pleistocene at least some humans regarded dogs not just materialistically, but had developed emotional and caring bonds for their dogs.[10]
First dogs as a hunting technology
Image on a Krater (vase) depicting a boar hunt in Ancient Greece
Ptolemaic mosaic of a dog and askos wine vessel from Hellenistic Egypt, dated 200-150 BC, Greco-Roman Museum of Alexandria, Egypt
During the late Paleolithic, the increase in human population density, advances in blade and hunting technology, and climate change may have altered prey densities and made scavenging crucial to the survival of some wolf populations. Adaptations to scavenging such as tameness, small body size, and a decreased age of reproduction would reduce their hunting efficiency further, eventually leading to obligated scavenging.[16][160] Whether these earliest dogs were simply human-commensal scavengers or they played some role as companions or hunters that hastened their spread is unknown.[16]
Researchers have proposed that in the past a hunting partnership existed between humans and dogs that was the basis for dog domestication.[161][162][163] The transition from the Late Pleistocene into the early Holocene was marked by climatic change from cold and dry to warmer, wetter conditions and rapid shifts in flora and fauna, with much of the open habitat of large herbivores being replaced by forests.[163] In the early Holocene, it is proposed that along with changes in arrow-head technology that hunting dogs were used by hunters to track and retrieve wounded game in thick forests.[162][163] The dog's ability to chase, track, sniff out and hold prey can significantly increase the success of hunters in forests, where human senses and location skills are not as sharp as in more open habitats. Dogs are still used for hunting in forests today.[163]
In Japan, temperate deciduous forests rapidly spread onto the main island of Honshu and caused an adaption away from hunting megafauna (Naumann’s elephant and Yabe’s giant deer) to hunting the quicker sika deer and wild boar in dense forest. With this came a change in hunting technology, including a shift to smaller, triangular points for arrows. A study of the Jōmon people that lived on the Pacific coast of Honshu during the early Holocene shows that they were conducting individual dog burials and were probably using dogs as tools for hunting sika deer and wild boar, as hunters in Japan still do today.[163]
Hunting dogs make major contributions to forager societies and the ethnographic record shows them being given proper names, treated as family members, and considered separate to other types of dogs.[163][164] This special treatment includes separate burials with markers and grave-goods,[163][165][166] with those that were exceptional hunters or that were killed on the hunt often venerated.[163][167] A dog's value as a hunting partner gives them status as a living weapon and the most skilled elevated to taking on a "personhood", with their social position in life and in death similar to that of the skilled hunters.[163][168]
Intentional dog burials together with ungulate hunting is also found in other early Holocene deciduous forest forager societies in Europe[169] and North America,[170][171] indicating that across the Holarctic temperate zone hunting dogs were a widespread adaptation to forest ungulate hunting.[163]
First dog breeds
Sled dog types, sketched in 1833
In 2017, a study showed that 9,000 YBP the domestic dog was present at what is now Zhokhov Island, arctic north-eastern Siberia, which was connected to the mainland at that time. The dogs were selectively bred as either sled dogs or as hunting dogs, which implies that a sled dog standard and a hunting dog standard existed at that time. The optimal maximum size for a sled dog is 20–25 kg based on thermo-regulation, and the ancient sled dogs were between 16–25 kg. The same standard has been found in the remains of sled dogs from this region 2,000 YBP and in the modern Siberian husky breed standard. Other dogs were more massive at 30 kg and appear to be dogs that had been crossed with wolves and used for polar bear hunting. At death, the heads of the dogs had been carefully separated from their bodies by humans, probably for ceremonial reasons.[64]
The study proposes that after having diverged from the common ancestor along with the grey wolf, the evolution of Canis familiaris proceeded in three stages. The first was natural selection based on feeding behavior within the ecological niche that had been formed through human activity. The second was artificial selection based on tamability. The third was directed selection based on forming breeds that possessed qualities to help with specific tasks within the human economy. The process commenced 40,000-30,000 YBP with its speed increasing with each stage until domestication became complete.
