We can easily imagine the way of life of humans during the Paleolithic. They had to chase their prey, move from place to place searching for areas with abundant food resources and shelter. They could not accumulate wealth and had to live in small groups, small enough to allow them to survive in an unpredictable environment. However, this way of life was deeply transformed by the domestication of plants and animals. Growing their own livestock and vegetables, primitive humans could predict resources available in the future. Larger cities could be established and a division of labor was possible, not everybody had to be involved in the production of food, and the first armies, bureaucrats and kings appeared. Consequently, the domestication of plants and animals has been considered the most important event in the last 15,000 years of human history(1).
Among all domestic species, both animals and plants, dogs (Canis familiaris) were the first ones to be domesticated. Bone remains show that at least 14,000 years ago dogs lived with humans in central Europe and the Near East(2,3). Consequently, the origin of the dog may have set the stage for the domestication of the other species and the change of our way of life. An understanding of the reasons that led to the origin of dogs, how, when and the place where it occurred, as well as the impact on the primitive societies, can be very important to be able to reconstruct the process of the domestication of other species.
We have been able to learn a lot about the origin of dogs thanks to many years of archaeological research. This research is based on the study of any sort of indication of historic and prehistoric association between dogs and humans. During the last 10 years, the development of molecular genetics techniques has opened a new field of research, complementary to the archaeological investigation, which can contribute to a better understanding of the origin of the dog. In this chapter I describe some molecular studies that have clarified a little bit when the process of the origin of dogs may have taken place. However, as we will see, these studies have not yet allowed a complete understanding of the domestication process and many questions remain to be answered.
MOLECULES VS. MORPHOLOGY
Two different approaches have been used to date the time when the origin of dogs took place. The first one is to try to identify bone remains whose morphology indicates that correspond to dogs and not to wolves (Canis lupus, the ancestor of the domestic dog). The second method consists in estimating the date when the mtDNA sequences present in dogs separated from the sequences in wolves. Although both methods target the moment when the dog and wolf lineages split, they look at different things and the dates obtained with both methods are expected to be different. To understand this, imagine one lineage that a certain time in the past splits in two, as indicated in Figure 1. This could correspond to the split of dogs from the ancestral wolf lineage, and the goal of the studies about domestication is to characterize when this separation occurred. Is at this point when the morphology of the two species starts to diverge. However, it will take some time for their morphology to be sufficiently divergent as to allow the unambiguous identification of bone remains as belonging to one species or the other. Zeder and Hesse(4) and Zeder(5) have shown that for other domestic mammals the morphological differentiation from the ancestor did not occur until some time after the initial domestication, when the domesticates expanded to neighboring areas where they could not mate with wild animals. Similarly, we could expect that the morphological change in dogs may have occurred some time after the domestication (although we do not know how much later). Since this is the kind of evidence used by archaeologists, and also because the ancient dog bone remains are very scarce, the dates of domestication based on archaeological data will tend to be more recent than the split between dogs and wolves.
Difference between the species divergence time, and the estimates obtained using genetic and morphological data. Species are indicated as gray bands, and the black lines represent the genetic relationships between sequences from each species. Morphological differentiation between species increases from the time of reproductive isolation.
Molecular estimates of the time of divergence are based on the comparison of DNA sequences. Applying a molecular clock it is possible to estimate the time necessary to make the two lineages as different as they currently are. In Figure 1, the mtDNA lineages present in wolves and in dogs are represented as the lines inside the gray area. However, the split of the lineages is necessarily older than the split of the populations (the domestication). Consequently, estimates of the date of the domestication based on DNA sequences may be older than the precise time.
In summary, while archaeological approaches may lead to an underestimation of the date of domestication, molecular methods tend to produce overestimates. While the search for old dog remains continues, molecular analysis methods are constantly improving, and integrating both approaches will lead us towards a more correct view of the domestication process.
THE TIME AND PLACE OF DOMESTICATION
Archaeological evidence. The archeological record suggests that the first domestic dogs were found in the Middle East and Central Europe about 14-15,000 years ago (2,3,6,7,8). Most early dogs are morphologically distinct from gray wolves. Often they are smaller in body size and have wider crania, a more prominent stop on the face and a shortened crowded jaw (7,9). The fact that these bones could be identified as belonging to dogs and not to wolves implies that the animals had been living with humans for a time period sufficiently long as to allow some morphological differentiation from their wild ancestor. The small body size of Asian wolves and the shared presence with early dogs of some traits led to the suggestion that Asian wolves are the direct ancestor of the dog(10). However, the oldest dog remains unmistakably identified so far have recently been discovered in western Russia(3) and date to 13,000 to 17,000 years before present. These early dogs do not show a reduction in body size when compared to the local populations of gray wolves and have cranial proportions similar to the Great Dane.
Molecular genetics. The first attempts to use molecular genetics to study the origin of dogs took place in the mid-1990s. Okumura et al.(11) were the first to sequence the control region of a large sample of dogs but focused on Asian dogs. These authors observed that the mitochondrial DNA sequences grouped into a discrete number of clades. Tsuda et al.(12) similarly studied a large sample of dogs from Asia, but also included some samples from wolves. Consequently, they were able to convincingly demonstrate a close relationship between wolves and dogs. The close relationship was confirmed in a study published at the same time(13), but in this study we also tried to use the molecular information to estimate the date of the dog's origin. Our study included 162 wolves from 27 populations from throughout Europe, Asia and North America and 140 dogs representing 67 breeds. As Okumura et al. did one year earlier, we observed that when constructing one evolutionary tree with all dog sequences, they clustered in just four groups (clades I to IV, Figure 2). One of these groups, clade I, contained most of the studied dogs, and a more recent study including more than 600 modern dogs(14) concluded that about 80% of them had sequences belonging to this clade. This large diversity could indicate that this group of sequences was the oldest one and thus its origin could correspond to the original domestication event.
Phylogenetic tree of wolf (W) and dog (D) mitochondrial DNA control region sequences (261 base pairs in length ). Dog haplotypes are grouped in four Clades, I to IV.
To try to estimate the date of the dog's origin we calculated, using the molecular clock, how much time would be necessary to reach that level of diversity starting from a single mtDNA sequence. We followed these steps:
1. We estimated the average sequence divergence between wolves and coyotes (Canis latrans) for the studied region of the mtDNA: 7.5%
2. Considering that the fossil record indicates that morphologically differentiated wolves and coyotes existed at least 1 million years ago (15), the rate of divergence (the molecular clock) can thus be estimated to be around 7.5% per million years.
3. The maximum sequence divergence for sequences belonging to clade I was estimated to be 1%. This could be used to calculate when the sequences from that clade started to diverge.
4. We confirmed that the rate of evolution was not significantly different for the different lineages. This implies that the same molecular clock could be used for all the sequences.
5. Since the rate of divergence was around 7.5% per million years, the estimated time needed to generate divergences up to 1% was ... 135,000 years!
The result of the study of Vilà et al.(13) has been taken as a firm date. However, that estimation was not presented with confidence intervals and these are usually large in this sort of estimates. Also, the region of the mtDNA studied may not be the best to apply a strict molecular clock. On the other hand, the results were very clear to suggest that the origin of dogs had to be much older than indicated by the archaeological record.
More recently, another attempt has been made to use dog mtDNA information to estimate when dogs appeared (14). These authors also focused on the diversity of clade I and concluded that the origin could have taken place more recently. These authors used a different model of sequence evolution and only considered the sequences in their sample that were currently present at each continent. Since they found the largest diversity in East Asia they concluded that this could have been the place of dog's origin. Looking at the average sequence divergence among clade I sequences in East Asia they estimated that the age of the clade was 41,000 years (standard error: ±4,000), supporting an origin much older than suggested by the bone remains as the previous study. However, they considered that it was possible that clade I did not derive from one unique domestication event and that several wolf lineages were involved. After arbitrarily subdividing clade I in smaller groups of sequences they estimated that those groups could have originated between 11,000 and 26,000 years ago. Despite this wide range of dates they suggested "an East Asian origin for the origin of the dog 15,000 years ago"(14). Their conclusions have a series of problems:
1. East Asia was suggested as the center of the dog's origin because of its higher diversity. However, whereas most of the samples from the rest of the world corresponded to purebred dogs, this region was characterized by mongrel dogs and dogs of non-recognized breeds. Obviously, these animals do not belong to inbred lines and may have a much higher genetic diversity, and this can bias the results.
2. The patterns of current diversity may be very different from ancestral patterns(16): looking at modern dogs may not be appropriate to reconstruct patterns of diversity that existed in one region in the past.
3. There is no objective evidence indicating if clade I derived from one or more founding wolf lineages. Subjectively dividing the clade in smaller groups can produce whatever result the researcher wishes to obtain.
4. Despite the fact that the date of origin that the authors obtain for one of their subclades is very old, 26,000 years (confidence interval: 18,000-34,000 years), they conclude that the origin of the dog took place about 15,000 years ago.
Although the results of this study apparently fit with the dates derived from archaeological remains, the conclusion that dogs could have been domesticated in East Asia 15,000 years ago faces one main problem: dog remains (already morphologically differentiated from wolves) of about that time have already been discovered in several places in Europe(3,6) and Asia(2,8), and probably also existed in America(16). The analysis of mtDNA sequences in pre-Columbian dogs of Leonard et al.(16) has shown that they clearly had Eurasian origin, implying that they arrived to the Americas with the first humans. Since all these dogs in Europe, Asia and America shared a common origin we can presume that the origin of the dog had to take place significantly before 15,000 years ago to allow their expansion over three continents.
The debate about the date of the origin of the dog is far from closed. The molecular analyses, more than clarifying the existing doubts, have opened new avenues for research. At this point, it seems clear that dogs had to be originated more than 15,000 years ago, as the traditional archaeological research suggested, but it is not clear how much earlier. However, this implies that man and dog may have lived together for some time at the end of the Paleolithic, forcing us to reconsider what we knew about the way of life of humans during that time and their expansion across continents. Archaeological and molecular approaches suffer different biases, but the combination of both approaches is most likely to provide a more clear view about the coexistence of dogs and humans.
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