Of Bonobos and Bottlenecks: Shifting Battle Lines in Dog Domestication Debates

A year ago I attempted to synthesize and, within my limited competence, comment upon archeological and genetic research regarding the origins of canine domestication.  This is not a static field and a number of papers that have appeared since show that the landscape continues to shift in significant ways.  The date of initial domestication of dogs has been pushed back to 32,000 years ago by one group (Wang et al. 2013), while analyses of the bones found in the Goyet Cave in Belgium and the Altai Mountains in Russia, dated respectively from 36,000 and 33,000 years ago, appear to contain DNA of animals that were more dog than wolf, or at least somewhere in between, though perhaps not ancestors of current dogs but rather “aborted domestication episodes”—animals that had begun relationships with humans but which did not survive the Last Glacial Maximum. 

There have been so many publications from different laboratories, with overlapping teams of researchers, that it is sometimes difficult to clearly identify the positions of the schools of thought on dog domestication.  Certain scientists appear on many papers, yet inconsistencies between the conclusions of those papers make it nearly impossible to determine what those scientists actually believe from moment to moment.  This is primarily a problem for amateurs such as myself, however, as the percolating nature of the research probably proves that dog domestication is truly one of the most exciting fields for a biologist, of whichever subdiscipline, to be working in. 

Where Domestication Occurred

Bone Pendant of Dog or Jackal (Anthropologie, 27, at 21)

In my March 2013 blog on the archeology and genetics of domestication, I found that a principal focus of debate between the major groups working in this area concerned the original locus of domestication, with arguments being presented primarily for East Asia and South China, the Middle East, and Europe.  This debate continues but no longer seems as heated a stretch of the battle line between the principal research teams. Consider the following statement in a review paper by Robert Wayne and Bridgett vonHoldt:

“Nuclear genetic evidence is consistent with European as well as Middle Eastern wolf populations contributing to the dog genome, whereas mtDNA evidence suggests an East Asian origin.  However, backcrossing to various wolf populations complicates a simple scenario for dog origins.” 

The statement that mitochondrial DNA evidence suggests an East Asian origin is at least a tentative acknowledgment of the work of Savolainen and others.  This tentativeness becomes even more pronounced deeper into the paper:

“The high degree of haplotype sharing among dog breeds and Middle Eastern wolves suggests an origin there or, as mentioned above, extensive backcrossing between Middle Eastern wolves and ancestors of modern and ancient dog breeds.  However, the similarity of some specific East Asian ancient breeds and Chinese wolves suggest that wolves from this area contributed to the dog genome as well…. Moreover, the significant component of haplotype sharing for 15-SNP [single-nucleotide polymorphism] windows implies both the Middle East and Europe may have contributed substantially to the genome of domestic dogs, a result that is consistent with the archeological record.”

Wolves on Stone and Bone (Capitan, Fig. 131)

Such openness to complexity in the locus of domestication is not shared by all researchers working in the area, and depending on what co-authorship means, may not be what Robert Wayne believes.  A paper analyzing complete mitochondrial genomes, Olaf Thalmann (2013), which had 30 co-authors, one of whom was Wayne, who was also a contact author, remains critical of arguments for a non-European location for the onset of domestication, stating that such research, particularly associated with Peter Savolainen, was “more limited in sampling of modern or ancient wolves or prehistoric dogs and had weak statistical support for phylogenetic branching points.”  While acknowledging that their own sampling “does not contain specimens from the Middle East or China, two of the proposed centers of origin,” the researchers argue that specimens from those regions are not older than approximately 13,000 years.  The paper states that “the mitochondrial legacy of dogs derives from wolves of European origin,” which is difficult to reconcile with the statement of Wayne and vonHoldt that “mtDNA evidence suggests an East Asian origin.” 

Genetics of Late Pleistocene Dog-Like Canids

Thalmann et al. analyzed the Goyet Cave canid, which was dated by Mietje Germonpre, one of Thalmann's co-authors, to 36,000 years ago.  The current team said that this animal’s “mtDNA relation to other canids places it as an ancient sister-group to all modern dogs and wolves rather than a direct ancestor of dogs.” Therefore, “the Belgian canids, including the Goyet dog, may represent an aborted domestication episode or a phenotypically distinct, and not previously recognized, population of gray wolf.” 

As to the wolf-like canid from the Altai Mountains, dated to 33,000 years ago and also discussed in the prior blog, the team, which also included Nikolai Ovodov, who first described the Altai specimen archeologically, classified it in the extant dog clade D, consisting at present of two Scandinavian breeds.  As to this clade, the paper states:

“The grouping of clade D with ancient wolf lineages and the association of the Altai specimen with this clade do not support recent common ancestry of the Altai specimen lineage with the great majority of modern dogs.  However, clade D dog haplotypes could have been captured as a result of interactions between ancient wolves and early humans that migrated into Scandinavia.”

The Altai dog is not described as ancestral to the extant Scandinavian breeds with which it shares a small clade. Is there a presumption that traits of the group of canids to which the Altai dog belonged were still breeding with wolves and that there is enough difference between the ancient group and the modern Scandinavian breeds that the connection is best explained by the mediation of wolves? In a paper concerning coat color to be discussed below (Ollivier et al.), something of the opposite (i.e., transmission from dogs to wolves) is used to explain the presence of black coat color in North American wolf populations.  Since Thalman et al. speculate that the Altai specimen may represent an “aborted domestication episode,” it should be explained why wolves would be more likely than proto-dogs to migrate to Scandinavia.  (See also the discussion of DNA haplogroup d1 in Klutsch et al. (2010).)

There is a bigger problem, however. A separate paper by Anna Druzhkova (2013) and a team that included Thalmann, Ovodov, and Wayne, and which was published barely six months earlier, reaches an inconsistent conclusion regarding the clade to which the Altai canid should be assigned.  Although stating that the specimen has “no perfect match to any extant dog or wolf,”  the earlier paper concludes that the Altai canid’s—

“haplotype cluster is embedded in a clade comprising exclusively contemporary dog sequences (Clade A) and contains the majority of dog haplotypes (45 out of 72) including diverse breeds such as Tibetan Mastiff, Newfoundland, Chinese Crested, Cocker Spaniel or Siberian Husky.”   This team concludes that “the Altai specimen is likely an ancient dog with a shallow divergence from ancient wolves. These results suggest a more ancient history of the dog outside the Middle East or East Asia, previously suggested as centres of dog origin.” 

The later paper makes no reference to the first though its supplementary materials cite it and allude rather obliquely to the discrepancy by stating that an “unambiguous delineation of the phylogenetic position of this Altai dog mtDNA as either dog or wolf is inconclusive…. Interestingly, the highest proportion of quartets supports a topology of the Altai dog clustering with other ancient canids to the exclusion of modern dogs and wolves, which is indicative of some shared mutations uniting all ancient canids. ” I was advised by one of the joint authors that the results of the Science paper, the team headed by Thalmann, are “more robust” than the earlier paper, so the Clade D affiliation is to be accepted for the moment.   

Wolves (Capitan, Fig. 132)

If the Goyet and Altai canids were more genetically like dogs than wolves, or at least in between, yet were also aborted domestication episodes, the fact that genetic changes could have parallels between humans and dogs (the evidence for which is discussed below) certainly suggests that genetic changes in aborted episodes could run parallel to changes in the successful domestication episode that eventually led to modern dogs.  This would not, of course, include those changes associated with the human development of agriculture, which did not occur before the Last Glacial Maximum when, presumably, lines including the Altai and Goyet dogs would have disappeared.  By taking both the Goyet and Altai canids out of most lines of subsequent canid groups, however, the dating of those bones remains primarily the province of paleontological techniques. 

Admixture of Wolf and Dog Populations

Adam Freedman and 29 colleagues (2014) sequenced wolf genomes from possible centers of the origin of canine domestication but “found that none of the wolf lineages from the hypothesized domestication centers is supported as the source lineage for dogs.” Greger Larson and Daniel Bradley, writing in the same issue of PLoS Genetics in which Freedman’s paper appears and introducing it, describe the use of whole genome sequences, also found in Thalmann et al., as “an exciting new phase” for genetic research on dog domestication. 

Freedman et al. state that post-divergence gene flow complicates the attempt to understand the separation of dogs from wolves, which they note is also a complicating factor in analyzing the relationship between and evolution of humans and Neandertals.  Gene flow between wolves and dogs is found by these researchers to have occurred in different parts of the world:

“We found significant evidence of admixture for three population pairs: Israeli wolf and Basenji, Chinese wolf and Dingo, and Israeli wolf and Boxer…. Care should be taken in interpreting these results, as the detected admixture signals may reflect gene flow between lineages ancestral to our contemporary samples. The signal for Chinese wolf and Dingo likely represents ancient admixture in Eastern Eurasia, and the signal observed for Israeli wolf, Basenji, and Boxer likely represents ancestral admixture that occurred in western Eurasia.”

The researchers also found “significant gene flow between the golden jackal and the Israeli wolf.”  They estimate a divergence time between 415,000 and 382,000 years “between the golden jackal and the population ancestral to dogs and wolves, which is considerably more recent than previously reported.”  The latter is a reference to Perini et al., 2010, which at Figure 4 graphically indicates the separation of the golden jackal (Canis aureus) from the wolf line as more than a million years ago. This result is also relevant to the work of Rueness et al. (2011) on Canis aureus lupaster, “the cryptic African wolf,” discussed in a prior blog.  

Freedman et al. argue that admixture with wolves may not have been adequately taken into account in prior research:

“[T]he presence of long shared haplotypes in Middle East wolves with several dog breeds may reflect historic admixture rather than recent divergence. Similarly, elevated genetic diversity in East Asian dogs and affinities between East Asian village dogs and wolves may be confounded by past admixture with wolves. In areas where village dogs roam freely and wolves have historically been in close proximity, admixture may also be present and exert a non-trivial impact on patterns of genetic variation.”

Distinguishing recent from ancient admixture (e.g., by the presence of long shared haplotypes) may become a major focus of research. The proponents of an East Asian origin will undoubtedly have to deal with this issue as well. 

Freedman et al. note that estimates of mutation rates vary considerably in different studies, describing this as “the dominant source of uncertainty in dating the origin of dogs.”  Their calculations used a mutation rate that argued for domestication between 16,000 and 11,000 years ago, but they note that if they accepted the mutation rate used by Wang et al., the event might have to be placed even earlier than the 32,000 year-ago domestication that team proposes. 

As to which wolf population domesticated dogs came from, Freedman et al. did not find that dogs diverged from any specific population, but rather that “dogs diverged from wolves at about the same time that the sampled wolf populations diverged from each other.”  Thus, dogs may have diverged from a population ancestral to modern wolves, but the team also accepts that dogs might have diverged from a now-extinct wolf population.  

Size of Founding Population and Bottlenecks

Niskanen et al. (2013), a team that included Peter Savolainen, attempted to estimate the size of the wolf population from which dogs arose and concluded that there were a minimum of 51 wolf founders but that the number was most likely larger, at least 500 animals. They argue that domestication “was not a very rapid or local process,” and elaborate:

“Possibly, domestication of wolf was a cultural process, which was spread across a large geographical area and involved many wolf populations. It has also been suggested that the domestication process was started by the wolves taking advantage of the food waste around villages—rather than by deliberate human action [citing the Coppingers]. If so, this behavior probably developed over a period of time and in an extended region.”

 
Wang et al, the team that pushed domestication back to 32,000 years ago, concludes that bottlenecks subsequent to domestication were rather mild, which the authors argue is consistent with “an evolutionary trajectory for dogs that is often called self-domestication,” again citing the Coppingers.  Although this paper does not refer to Niskanen et al., the team that concluded that the number of wolf founders was probably at least 500 animals, both papers had Peter Savolainen as a co-author and presumably can be correlated to some degree. Such a small founding population would have had to expand before a severe bottleneck could be tolerated.   

Freedman et al., who, as discussed above, date the divergence of wolves from dogs at about 15,000 years ago, reach dramatically different conclusions on founding numbers and bottlenecks.  This team states that their “results indicate the ancestral wolf population from which dogs were domesticated was considerably larger than estimated from current levels of diversity in wolves.”  They believe that the population ancestral to both dogs and wolves numbered about 45,000 individuals, but that following the separation there was a 3.6 fold reduction in the number of wolves to about 12,600 individuals but a 22-fold reduction in the population ancestral to all dogs of only 2,000 individuals.  They note that these bottlenecks are more severe than previous estimates of a two- to four-fold reduction in the dog population, referring to Lindblad-Toh et al. (2005) and Gray et al.  Lindblad-Toh found that modern dog breeds “are the product of at least two population bottlenecks, the first associated with domestication from wolves (~ 7,000—50,000 generations ago) and the second resulting from intensive selection to create the breed (~ 50—100 generations ago).”  Gray et al. similarly “found evidence for a modest population contraction ~ 15,000 years ago (5000 generations ago) and severe contractions at breed formation.” 

Thalmann et al., which shares three co-authors with Freedman, including Wayne, though only speaking about one clade (A, the largest in terms of breeds), states:

“A Bayesian Skygrid analysis applied to the largest clade (A), found a continuous population increase from the most recent common ancestor of the group, approximately 18,800 years ago, to about 5,000 years ago, followed by a decline from 5,000 to 2,500 years ago, and then a sharp increase in population size correlating with the increase in the human population.  The paper states that this “suggests demographic dependence of dogs on human populations.  In contrast, wolf numbers declined during this period, consistent with the emergence of agrarian cultures and the loss of vital wolf habitat and wild game.” 

Determining the size of the ancestral wolf population from which dogs arose must, in the end, not be merely a matter of the mathematics of genetics. If that population was 500 and occurred 32,000 years ago or 2,000 and occurred 15,000 years ago, one must still explain the environmental context in which such a number of individuals began to go in a separate direction from a group that remained wild. If self-domestication was the behavioral mechanism at a time when human groups were relatively small bands of hunters, how many such bands would have to be involved, over how large an area?  Were these bands essentially sedentary, living in caves over many generations, or were migratory patterns involved that spread the tamer wolves to other groups? Perhaps the proto-dogs were domesticating themselves not just as a matter of stabilizing their relationships with humans but also in order to be more cooperative with each other, as happened in the intraspecific behavior of bonobos after they separated from chimpanzees, as will be discussed below. 

Southeast Asia as a Secondary Locus of Canine Expansion

Benjamin Sacks, Sara Brown and four others (2013) note that dogs are “an especially valuable proxy for understanding Holocene human movements,” but note that inconsistent faunal and DNA remains, which can be combined with canine data, “have limited our understanding of phylogeography of the earliest dogs.”  They accept the conclusion of Savolainen and others that “worldwide analyses of mtDNA indicate that modern dog matrilines reflect a subset of those found today in Southeast Asia.”  The Southeast Asian origin theory can, however, be refined:

“If, however, dogs were absent from Southeast Asia until the Neolithic, the most parsimonious hypothesis reconciling archeological and mtDNA observations would be that early dogs entered Southeast Asia with pre-Neolithic peoples from the west or north, then later expanded outward 8–5 Ka [thousand years ago] swamping or replacing more primitive dog populations. Several lines of evidence support such a ‘Neolithic replacement’ hypothesis. First, Neolithic expansion of dogs from Southeast Asia 8–5 Ka would be in line with linguistic, cultural, archeological, and human genetic evidence of a westward expansion of Neolithic humans from the Yangtze and Yellow River basins … , the precursor to the slightly later migrations of Austronesian-speaking farmers from this same region, which were responsible for spreading dogs to Island Southeast Asia and Oceana.”

This team calls this the Neolithic Replacement hypothesis, to be contrasted with a Southeast Asian Origins hypothesis.  Thus, they see Southeast Asia as “a secondary center of diversification associated with Neolithic rather than Paleolithic peoples.”  They describe this secondary expansion as “massive,” and argue that the Southeast Asian dogs were able “to demographically dominate and largely replace earlier western forms.”  (This might be comparable to the large-scale replacement of pre-Colombian American dogs with European dogs discussed below.) The researchers believe this transformation could have been central to the evolution of dog diversity. 

“[T]he dogs of southern China could have been the first large population to have been reproductively isolated from wolves (Canis lupus), possibly accelerating their phenotypic divergence and diversification as a domesticate. Rapid spread of such a [southern Chinese] dog in combination with interbreeding with ancient western dogs could have produced a variety of forms, laying the basis for the first ancient regional breeds, which were first evident approximately 8,000 years ago.” 

Apparently “ancient western dogs” were not reproductively isolated from wolves.  Are we to imagine that the Goyet and Altai dogs were such dogs?  In any case, the Neolithic Replacement hypothesis could arguably receive archeological support from the dog burial research of Losey et al., discussed several sections below.    

Genetic Changes During Domestication  

Wang et al. (2013), already mentioned as having used genetic evidence to date domestication at 32,000 years ago, state that “Chinese indigenous dogs are likely one of the early groups that resulted from the first stage of dog domestication and were subsequently the source from which dog breeds were further selected,” but nevertheless concede that “the ancestral Chinese wolf, from which domesticated dogs may have originated, may already be extinct.  In addition, several wolves from Europe and Mexico are closer to dogs than the Middle-Eastern wolves … , thus, it may be difficult to use patterns from extant wolves to infer domestication location.”  This seems to reflect the willingness noted at the beginning of this blog to move the debate on domestication away from one primarily about location.   This team speculates on what the earliest domesticated populations were doing for men in the 20,000 years before agriculture arose:

Wolf from Laugerie-Basse (Anthropologie, 27, at 16; Paillet, Figs. 10, 11)

“Early wolves might have been domesticated as scavengers that were attracted to live and hunt commensally with humans. With successive adaptive changes, these scavengers became progressively more prone to human custody. In light of this view, the domestication process might have been a continuous dynamic process, where dogs with extensive human contact were derived from these scavengers much latter when humans began to adopt an agricultural life style.”

Wang et al., describing the “striking parallelism in the recent evolution of dogs and humans,” find genes apparently selected for in both dogs and humans “specifically for sexual reproduction, digestion and metabolism, and neurological processes.” Also, many cancer-related genes are shared by both species.  They note that genes associated with nerve cells were selected, and citing Belyaev’s work on foxes, state: “Strong selection on behaviour (for example, reducing aggression) and neurological traits (for example, complex interactions with human beings) is often involved in the first steps of animal domestication.”  A gene for a membrane protein that transports the neurotransmitter serotonin, variations of which lead to aggressive behavior, obsessive-compulsive disorder, depression, and autism, is found in both species. 

“Most interestingly, dogs respond similarly to the drugs that are used to treat humans (for example, clomipramine hydrochloride, a serotonin-reuptake inhibitor often also used as an anti-depressant drug), suggesting possible common genetic components for these behaviours in humans and dogs…. The protein coded by SLC6A4 might underlie the genetic component of many neurological traits in both dogs and humans.” 

The authors indicate that a possible explanation of the need for neurological change might relate to the population density resulting from domestication:

“As domestication is often associated with large increases in population density and crowded living conditions, these ‘unfavourable’ environments might be the selective pressure that drove the rewiring of both species. Positive selection in neurological pathways, in particular the serotonin system, could be associated with the constant need for reduced aggression stemming from the crowded living environment. Moreover, the complex intimate interactions between dogs and humans might have also driven some of the striking parallelism seen in these two species.”

The similarity of diseases between both species might be worth studying more as this could “shed light on the genetic architecture of these disorders in humans.” Unfortunately, this may imply more pharmaceutical research using dogs as laboratory animals.  

Axelsson et al. (2013), discussed in a prior blog, had concluded that dogs, during the human development of agriculture, adapted to “thrive on a diet rich in starch, relative to the carnivorous diet of wolves.”  Wang et al., referring to this research, note that genes having roles in the selective transport of dietary cholesterol were affected in both humans and dogs.  “As domestication has led to drastic changes in the proportions of plant food, relative to animal food, natural selection on these genes in both species is expected due to this shared evolutionary history.”

Wolves (Capitan, Fig. 131)

Yan Li and six colleagues (2013), including Bridgett vonHoldt and Robert Wayne, found that during domestication genes expressed in the brain evolved rapidly, “consistent with the evolution of dog-specific behaviors during domestication.” They elaborate:

“The primary key for early domestication is the transformation of negative defensive reactions toward humans (the fearful-aggressive response) to positive reactions, which means physiological changes in the systems that govern neurochemical production …. Specifically, such physiological change has been characterized by fearful response and a reduced locomotion in a novel environment and increased glucocorticoids that regulate the fear response by mediating neurotransmitter serotonin metabolism ….  The behavior evolution is mostly attributable to brain evolution.”

Freedman et al., already discussed regarding the wolf population in which domestication began, also refer to Axelsson’s research regarding the genetic changes in dogs correlating with the human development of agriculture.  This team, however, focused specifically on the AMY2B gene, encoding alpha-2B-amylase. They report that the Dingo has just two copies of the gene, “suggesting that the AMY2B copy number expansion was not fixed across all dogs early in the domestication process.”  The team also says that the Siberian Husky, “a breed historically associated with nomadic hunter gatherers of the Arctic, has only three to four copies of AMY2B, whereas the Saluki, which was historically bred in the Fertile Crescent where agriculture originated, has 29 copies.” 

It can be expected that an ever more detailed picture of the genetic stages during domestication, with correlations to behavioral and environmental changes, will begin to emerge in the coming years. 

Behavioral Changes During Domestication

An international group of behavioral scientists headed by Bridgett Waller finds that dogs with facial expressions that enhance their neonatal appearance were preferentially selected by humans visiting shelters.  This team (Waller et al. 2013) summarizes prior research establishing that in “many ways dogs appear more like wolf puppies than wolf adults.”  Among features making dogs look more like wolf puppies than adults are shorter snouts, wider craniums, upper face facial muscle contractions that increase the apparent size of the animal’s eyes, and other submissive behaviors such as tail wagging.  Using shelter dog adoptions as a proxy for dogs’ selection by humans over evolutionary time, these researchers “tested whether humans (when adopting dogs from a shelter) actively select for dogs, which appear more juvenile in the face as a result of facial muscle contraction.”  Facial movements were analyzed under the Facial Action Coding System (FACS) developed by other researchers for use across species, and specially adapted for dogs under the name DogFACS.  (See Ekman et al., 2002, for an overview of FACS.) 

These researchers found that dogs that produced a high frequency of facial movement to raise the inner brow were adopted more quickly from shelters and conclude that “this suggests that dogs have evolved to manipulate the human preference for paedomorphic features using the face.”  Curiously, excessive tail wagging did not help dogs but actually hurt their chances, suggesting that “indirect manipulation of human sensory preferences (particularly a preference for juvenile facial characteristics) has been a particularly powerful selective force in domestication.”   

The team finds that facial expressions that were effective also make the dogs look sad, so that the adopters may have been responding to perceived sadness.  They argue, however, that sadness expressions may be paedomorphic in humans, a means of displaying vulnerability.  “We can therefore speculate that early domestication of wolves may have occurred not only as wolf populations became tamer, but also as they exploited human preferences for paedomorphic characteristics.” 

A recent paper that concerns bonobos rather than dogs is important in connection with behavioral changes during domestication.  Brian Hare et al. (2012) considered the lower level of aggression demonstrated by bonobos (Pan paniscus) than is found among chimpanzees (Pan troglodytes).  They state that the two species diverged about a million years ago, but that bonobos had more plentiful feeding areas and did not have to compete with gorillas for resources.  In this environment, females formed strong coalitions with one another, these coalitions thwarted male efforts to dominate females, less aggressive males allied with female relatives, males with more juvenilized adult aggressive behavior were favored, and other changes had a cascading effect “as in human-driven domestication.”  This suggests that not only must the interspecific communication of dogs and humans be considered in analyzing behavioral changes during domestication, but attention must also be given to intraspecific communication.  Using the Coppingers’ self-domestication model, when dogs began to live near dung heaps on the edges of villages, they presumably were more stationery and in closer proximity to each other for longer periods of time, during which their relationships were slowly transformed. Perhaps some level of instraspecific change had to occur before the first animal was brought into the camp.

That intraspecific factors must have been involved in the self-domestication of dogs is arguable from the size of the founding population hypothesized by Freedman et al. (2,000, after a bottleneck following separation from a wolf population of about 45,000 individuals), or even Niskanen (probably 500, but perhaps as few as 51).  Although it is easy to imagine 51 wolves becoming camp followers to a few bands of humans, larger numbers might require an additional explanation.  Alteration of intraspecific behavior with reduced aggression and accompanying morphological changes (per Belyaev's foxes) seems likely to have been critical in the domestication process.  

Arctic Breeds, Chihuahuas, and Carolina Dogs Keep Pre-Colombian Markers

The difficulty of finding genetic evidence concerning pre-Colombian American dogs was discussed in a prior blog, but recent research has made dramatic headway in this area.  Barbara von Asch et al. (2013), in a team that included Peter Savolainen, summarize prior research on pre-Colombian dogs by stating that such “dogs must have been brought along by Paleo-Indians of Asian origin in their expansions throughout the American continent, although not necessarily in connection with the first waves of humans.” The question this group posed was as follows: 

“Did the ancient migrants leave descendants in the modern American gene pool or were they completely erased by European dogs brought across the Atlantic in the post-Columbian era, and are extant dog populations direct descendants of the ancient populations in the same geographical region?”

The researchers find that “Inuit sled dogs, Canadian Eskimo dogs and Greenland dogs had similar mtDNA gene pools.”  They find evidence that the modern Alaskan Malamute descended from the pre-European Alaskan population, but note that a particular haplotype (A29) was shared with the Siberian husky with which Alaskan huskys were interbred in the early 1900s. They also describe the results for the Malamute as “ambiguous,” apparently because of this interbreeding.  The researchers state that the presence of the A29 haplotype (absent in Europe) indicates genetic links between East Asia, Siberia and Arctic America.   They find that the “Alaskan Malamute and the Eskimo/Greenland/Inuit group had almost totally different mtDNA gene pools.”  The researchers conclude that the Inuit/Eskimo/Greenland group “have remained practically uninfluenced by European lineages.” They also note that the “total lack of shared haplotypes” between the two broad arctic groups “possibly reflects sequential arrival to America of the related human populations.” 

The researchers found a haplotype (A185) unique to Chihuahuas among modern dogs.  A185 was found in one pre-Colombian sample from Mexico “suggesting direct ancestry of Chihuahua from ancient Mexican dogs.”  The Mexican xoloitzcuintle (xolo) had “only haplotypes occurring universally and two haplotypes found in Europe.”  The Peruvian perro sin pelo del Peru included individuals with haplotypes unique to Europe but shared a haplotype with the xolo.  The Paulishtinha and dog Argentino breeds were believed to “originate from dogs of known European ancestry… and carried only haplotypes that are frequently found in Europe.” 

A haplotype (A184), unique to Carolina dogs among American breeks, is described by the researchers as belonging to an East Asian-specific phylogenetic subclade.  The researchers conclude that this and the presence in one individual of a haplotype found only among Chinese non-breed dogs and the Japanese shiba inu, “gives strong support to the hypothesis that the Carolina dog has indeed originated from pre-Colombian dogs.”  South American free-ranging dogs, however, were found likely “to originate mainly from European dogs, although traces of native dogs cannot be totally excluded.” 

The overall conclusion of the research was that “all ancient American sequences except one (D40; possibly the result of dog-wolf crossbreeding) can now be linked to haplotypes present in East Asia or Siberia.” That there was dog-wolf crossbreeding in the Americas is indicated in the next paper discussed.

Coat Color Variation Appears in Dogs

Font de Gaume Wolf (Capitan)

Morgane Ollivier and 14 colleagues (2013), looking at two genes controlling coat color in 68 dogs and wolves from 28 different archeological sites in Asia and Europe, ranging from 12,000 to 4,000 years ago, find that an allele that causes melanism and a variant that may cause light hair color, were present as early as the beginning of the Holocene, over 10,000 years ago.  In the introduction to the paper, the researchers state that the diverse locations where early dogs have been excavated “had no cultural ties.”  They add that “several populations of wolves may have been at the origin of these domestication events and early dogs were probably characterized by significant genetic variability.”

The genes studied by this group, Mc1r and CBD103, are “implicated in coat color variation,” regulating the production of red/yellow versus brown/black pigment.  A particular mutation is currently only found in the Mc1r sequences of Siberian Huskies and Alaskan Malamutes.  The mutation was found in ancient dog samples in Asia and Southeastern Europe, but not Western Europe.  Where a particular allele was dominant, coat color was, the authors hypothesize, black.  They state that “this mutation and the subsequent black phenotype have been present in the dog for 8,000 years at least.”  They give a date range of 11,000 to 8,000 years ago for the first occurrence of this mutation in Eurasia.  They state that their results are “congruent” with prior results indicating that the mutation is at least 46,886 years old, but do not explain how congruence to a change 35,000 years earlier is to be understood. 

Melanism is found only in North American and Italian wolves.  In Italy, this team accepts that the transfer arose from recent hybridization between wolves and free-ranging dogs.  In America, however, Ollivier et al. believe the “data would suggest that early black dogs of Eurasia could have migrated since the Upper Palaeolithic to North America across the Bering Strait and be at the origin of the present-day American black wolf populations, via a back-crossing process with local wolves.” 

Dog Burials in Siberia

Lake Baikal above Mongolia (Wikipedia)

One of the criticisms of the hypothesis for domestication in Asia has been that it does not square with the archeological record.  There may, however, be a tendency to get closer to Asia with some recent research in Siberia, though as already mentioned, the archeological research might also be consistent with the Neolithic Replacement hypothesis.  Robert Losey and nine colleagues (2013) wanted to know if dog burials on the shores of Lake Baikal in Siberia “could be related to the particular ways in which dogs were utilized by people in the past.” 

Canid burials first appear in the region “near the Mesolithic/Early Neolithic transition,” 8,000 to 7,000 years ago, beginning with a wolf, but followed several centuries later by a number of dogs. Dog burials appear at the same time as human graves and cemeteries become common in the area.  A dog buried between 7,420 and 7,325 years ago was found in a grave of an adult male human.  A dog buried from 7,150 to 6,945 years ago was placed in a sitting or crouching position.  One dog, buried between 6,880 and 6,755 years ago “was interred wearing a necklace of eight red deer canine tooth pendants and also associated with its skeleton were a Bovidae scapula and horn core, two whole roe deer antlers, and other unidentified bones.”   The paper contains excellent drawings and photographs of these burials.  The researchers conclude:

“Dogs were the only domesticated animals living with humans at this time, and it appears that dogs and animals such as bears were considered by foraging groups here to be spiritually similar to humans, as were many animals among historic northern indigenous groups. When these broader beliefs were combined with intimate personal relationships with dogs, which here involved sharing many of the same foods, and the broader practice of burying one’s group members in cemeteries, some dogs were given ‘human’ mortuary rites.”

The dogs “had variable diets, with some relying heavily on aquatic foods, others much less so.”  The dogs “were eating much like the local humans who were most reliant on aquatic foods.”  The humans dogs were associated with, however, did not all have aquatic-food diets.  The authors conclude:

“Clearly, no single human subsistence practice or diet is correlated with the practice of burying dogs in Cis-Baikal. If anything, dogs were more commonly buried where diets were broader as a result of use of both terrestrial and aquatic fauna.”  The researchers speculate that humans may sometimes have kept larger fish for themselves, and given smaller fish to dogs. 

Dog burials found so far are concentrated in the Early Neolithic, but were absent in the Middle Neolithic and rare thereafter.  As to the pastoralists of the Late Holocene, the authors state:

“Pastoralist groups by definition lived in close association with many domesticated species, here most often sheep, goats, horses, and cattle. These groups regularly rode, sold, traded, sacrificed, and consumed these animals, and considered them property. Perhaps because dogs in these societies no longer had the unique position of being humans’ only cohabitant animal, and because people’s relationships to animals more broadly had changed with the emergence of pastoralism, dogs no longer were considered to have spiritual equivalency with humans and were no longer considered eligible for burial in human cemeteries.”

Conclusion

Reindeer Bone with Fox Head (Capitan, Fig. 131)

I can add but one suggestion for further research, which is that among the archeological data in need of reanalysis are certain caves and other locations of rock art, some of which date to the Upper Paleolithic.  Early analysis of canids depicted in such locations assumed that the animals could not be dogs because of the dating. (H. Breuil, Anthropologie 27, p. 595: “Étant donné l'âge des peintures, ce n'est pas admissible,” though Breuil considered the issue open. See Paillet and Man-Estier (2011) for rediscovery of items from the early digs.)  Figures that look like dogs could thus be labelled wolves or even hyenas a century ago, as was the case with the first figure above.  For the significance of this item and its likely depiction of a dog I am indebted to Don Hitchcock (personal communication and Megalithic Portal website). The other figures included in this blog are from the early twentieth century and were labeled as wolves or foxes but, under the timelines accepted by the research discussed here, might just as well be dogs.  If humans were burying dogs, would it not be likely that they were also drawing them on rocks?

Although it appears that most geneticists are willing to accept some level of domestication for the dog-like canids found in the Goyet Cave and the Altai Mountains, these animals appear to be aborted domestication events.  Current dogs, for most geneticists, appear to reflect a divergence from wolves of about 15,000 years ago, though one team now pushes the domestication event back to 32,000 years ago.  This date, however, assumed a mutation rate that has been rejected by a team that would date domestication more recently.  Research on mutation rates will be a major focus in the coming years, and may alter already published estimates of significant genetic events.  


"The presence of 

That dogs arose from wolves is no longer disputed, but where this occurred remains in doubt.  Although the various schools still plant flags on maps, there seems to be a growing acceptance that this issue is complicated and that conflicting data may have to be amalgamated, probably including findings that have yet to be made.  The wolf population from which dogs arose may have been confined to one region but the extent of the region is unclear and the size of the founding group is a matter of dispute.  The level of gene flow after domestication is a complicating factor in determining the date and place of domestication, and further research on wolf populations is likely to adjust the significance of current genetic evidence.  Findings from different research groups on bottlenecks in both wolf and dog populations cannot be reconciled at present. 

An area of dramatic development in the last two years concerns genetic and behavioral changes associated with domestication.  Regardless of when and where domestication began, it appears that dogs and humans underwent genetic alteration as they began living and cooperating with each other, and that some of these changes ran in parallel.  Areas showing overlap include neurological mechanisms, digestion and metabolism, and even disease.  Dogs became smaller than their wolf progenitors, and by the beginnings of agriculture if not earlier, began to look different from them in terms of coat color. 

The excavation of burial sites near Lake Baikal suggests that even before agriculture dogs were sufficiently important to receive human-like burials in Asia, sometimes with humans with whom they had been associated.  The effort to correlate archeology with genetics may often be fruitless, but must continue to be made, as was done by Larson et al. in 2012.  As Wayne and vonHoldt said in their review paper discussed at the beginning of this blog, it "is truly an exciting time for canine evolutionary genomics."

Thanks to Richard Hawkins and Kingsbury Parker for suggestions.  

Sources:

1. Axelsson, E., Ratnakumar, A., Arendt, M-J., Maqbool, K., Webster, M.T., Perloski, M., Liberg, O., Arnemo, J.M., Hedhammar, A., and Lindblad-Toh, K., (2013). The Genomic Structure of Dog Domestication Reveals Adaptation to a Starch-Rich Diet. Nature (published first online); doi:10.1038/nature11837.
2. Bourlon, Le Capitaine (1916).  Nouvelle Decouvertes a Laugerie-Basse. L’Anthropologie, 27, 1-26.
3. Capitan, L., Breuil, H., and Peyrony, D. (1910). La Caverne de Font-de-Gaume.  A. Chene, Monaco.
4. Coppinger, R., and Coppinger, L. (2001). Dogs: A Startling New Understanding of Canine Origin, Bheavior and Evolution. New York: Scribners.
5. Drake, A.G., Coquerelle, M., and Colombeau, G. (2015).  3D Morphometric Analysis of Fossil Canid Skulls Contradicts the Suggested Domestication of Dogs during the Late Paleolithic.  Scientific Reports (online February 5, 2015). This research is referenced here, though not included in the original analysis, for the observation that the Eliseevichi and Goyet "canid skulls share with wolves a lack of a pronounced stop," but this characteristic is seen in Neolithic specimens.  See the comments below on Paillet and Man-Estier (2011). 
6. Druzhkova, A.S., Thalmann, O., Trifonov, V.A. et al. (2013). Ancient DNA Analysis Affirms the Canid from Altai as a Primitive Dog.  PLOS ONE 8(3), e57554.   
7. Ekman, P. Friesen, W.V., and Hager, J.C. (2002). The Facial Action Coding System.  Salt Lake City, Research Nexus.
8. Freedman A.H., Gronau, I., Schweizer R.M., Ortega-Del Vecchyo, D., Han, E., et al. (2014). Genome Sequencing Highlights the Dynamic Early History of Dogs. PLoS Genetics 10(1). e1004016.
9. Gray, M.M., Granka, J.M., Bustamante, C.D., Sutter, N.B., Boyko, A.R., Zhu, L., Ostrander, E.A., and Wayne, R.K. (2009). Linkage Disequilibrium and Demographic History of Wild and Domestic Canids.  Genetics, 181(4), 1493-1505.
10. Hare, B., Wobber, V., and Wrangham, R. (2012). The Self-Domestication Hypothesis: Evolution of Bonobo Psychology Is Due to Selection against Aggression.  Animal Behaviour, 83(3), 573-585.
11. Hitchcock, D. posting on Megalithic Portal, identification of canid on pierced stone found at Laugerie-Basse (Aquitaine: Dordogne) as possibly a dog.
12. Klutsch, Seppala, Fall, et al. (2010). Regional Occurrence, High Frequency but Low Diversity of Mitochondrial DNA Haplogroup d1 Suggests a Recent Dog-Wolf Hybridization in Scandinavia.  Animal Genetics, 42(1), 100-103.
13. Larson, G., and Bradley, D.G. (2014).  How Much Is That in Dog Years?  The Advent of Canine Population Genomics.  PLoS Genetics, 10(1), e1004093.
14. Larson, G., Karlsson, E.K., Perri, A., et al. (2012). Rethinking Dog Domestication by Integrating Genetics, Archeology, and Biogeography. Proceedings of the National Academy of Sciences, 109(23), 8878-83.
15. Li, Y., vonHoldt, B.M., Reynolds, A. et al. (2013). Artificial Selection on Brain-Expressed Genes during the Domestication of Dog. Molecular Biology and Evolution, 30(8), 1867-1876.
16. Lindblad-Toh, K., Wade, C.M., Mikkelsen, T.S., Karlsson, E.K., Jaffe, D.B., Kamal, M., et al. (2005). Genome Sequence, Comparative Analysis and Haplotype Structure of the Domestic Dog. Nature, 438(8), 803-819.
17. Losey, R.J., Garvie-Lok, S. Leonard, J.A., Katzenberg, M.A., Germonpre, M., Nomokonova, T., Sablin, M.V., Goriunova, O.I., Berdnikova, N.E., and Savel’ev, N.A. (2013). Burying Dogs in Ancient Cis-Baikal, Siberia: Temporal Trends and Relationships with Human Diet and Subsistence Practices.  PLos One, 8(5), e63740.
18. Niskanen, A.K., Hagstrom, E., Hohi, H., et al. (2013).  MHC Variability Supports Dog Domestication from a Large Number of Wolves: High Diversity in Asia.  Heredity, 110, 80-85.
19. Ollivier, M., Tresset, A., Hitte, C. et al. (2013). Evidence of Coat Color Variation Sheds New Light on Ancient Canids. PLoS One, 8(10), e75110.
20. Paillet, P., and Man-Estier, E. (2011). Oeuvres d'Art Meconnues de Laugerie-Basse (Dordogne). Collection Capitaine Maurice Bourlon-Institut de PaleontologieHumaine, Paris.  L'Antrhopologie, 115, 505-521) ("Les représentations de Canidés, et plus spécifiquement de caninés, sont très rares dans l’art paléolithique. Leur détermination n’est pas toujours aisée." As to Fig. 11, a new drawing of the item in the fourth picture here, these authors note: "Le stop est bien marqué et le front bombé," yet they put a question mark after their designation of 'loup?', without stating any possibility that it might be a dog. Dr. Germonpre pointed out to me the stop and the swollen frontals of this animal, which could argue that it is a dog rather than a wolf. I believe that the same could be said of the canid on the pendant in the first picture here, as well as the left figure in the fifth picture and the Font de Gaume wolf.)
21. Perini, F.A., Russo, C.A.M., and Schrago, C.G. (2010). The Evolution of South American Endemic Canids: A History of Rapid Diversification and Morphological Parallelism.  Journal of Evolutionary Biology, 23(2), 311-322.
22. Riede, F. (2011).  Adaptation and Niche Construction in Human Prehistory: A Case Study from the Southern Scandinavian Late Glacial.  Philosophical Transactions of the Royal Society B, 366, 793-808 (Noting that arguments for domestication in China 16,300 years ago "stands in direct opposition to reports of domesticated dogs in the Upper Paleolithic," Riede suggests that "these seemingly opposing positions can be reconciled.  Bheavioural, morphological and genetic markers of domestication are not linked in a lock-step fashion.  The presence of C. familiaris in a range of Late Glacial archaeological sites in northern Europe indicates that, at the very least, these hunter-gatherer groups were beginning to engage in symbiotic relations with wolves. Possibly,these early breeds never became fully (i.e. genetically) domesticated.  Alternatively, breeds broughtto Europe by dispersing farming populations later replaced these earlier lineages.").
23. Sacks, B.N., Brown, S.K., Stephens, D. (2013).  Y Chromosome Analysis of Dingoes and Southeast Asian Village Dogs Suggests a Neolithic Continental Expansion from Southeast Asia Followed by Multiple Austronesian Dispersals.  Molecular Biology and Evolution, 30(5), 1103-1118.
24. Thalmann, O., Shapiro, B., Cui, P., et al. (2013). Complete Mitochondrial Genomes of Ancient Canids Suggest a European Origin of Domestic Dogs. Science, 342 (6160), 871-4.
25. Tito, R.Y., Belknap III, S.L., Sobolik, K.D., et al. (2011). Brief Communication: DNA from Early Holocene American Dog.  American Journal of Physical Anthropology, 145, 653-7.
26. von Asch, B., Zhang, A.-b., Oskarsson, M.C.R., Klutsch, C.F.C., Amorim, A., and Savolainen, P. (2013). Pre-Colombian Origins of Native American Dog Breeds, with Only Limited Replacement by European Dogs, Confirmed by mtDNA Analysis, Proceedings of the Royal Society B. 280: 20131142.
27. Waller, B.M., Peirce, K., Caeiro, C.C., Scheider, L., Burrows, A.M., McCune, S., and Kaminski, J. (2013). Paedomorphic Facial Expressions Give Dogs a Selective Advantage.  PLoS One, 8(12), e82686.
28. Wang, G-d, Zhai, W., Yang, H-e, et al. (2013). The Genomics of Selection in Dogs and the Parallel Evolution between Dogs and Humans.  Nature Communications, 4:1860.
29. Wayne, R.K., and vonHoldt, B.M. (2012). Evolutionary Genomics of Dog Domestication.  Mammalian Genome, 23(1-2), 3-18.