6
Let the Bones Speak
At some point in the past the lives of wolf and human became intertwined and it is from this partnership that the dog eventually emerged. Until genetics entered the fray, the only way of following this transition through the intervening millennia was through fossils. Good fossils are in short supply and the fossil record is understandably full of gaps.
In terms of time, the oldest skulls that could even remotely be differentiated from wolves were excavated in the Goyet cave in southern Belgium in the 1860s. Like all good fossil sites, Goyet is a limestone cave whose alkaline environment helps to preserve the calcified bones and, importantly, any DNA that might lie within.
From studying the style of stone and bone tools found there, it was clear that the cave had been occupied by humans for a very long time. Neanderthals lived there during the time of the Mousterian culture, which lasted from about 160,000 years to 40,000 years BP (the standard archaeological abbreviation for ‘before present’). It takes its name from the rock shelter at Le Moustier in the Dordogne region of central France. The Mousterian lasted until the arrival of modern humans, our ancestors, about 40,000 years ago. As is not uncommon with early excavations, disturbance of the layers within the cave made precise stratigraphic dating of the different artefacts found there problematic. However, carbon-dating of the fossils gave precise dates for the organic remains at least. The cave fauna was a rich assemblage of cave bear, cave lion, horse, reindeer, lynx, red deer and mammoth. In the deeper recesses of the cave archaeologists found the skull of a ‘large canid’ carbon-dated to 31,700 years BP. Was it a wolf or was it a dog?
Of course, there must have been a period after the first wolf was adopted into a human band when its skull was exactly the same as a wolf’s – because it was a wolf. There was no exact moment of transition from one to the other, and the whole debate has a strong flavour of semantics. The more cautious authors merely refer to these intermediates as ‘canids’ or ‘wolf-dogs’, thereby sidestepping the argument altogether.
A similar conundrum faced archaeologists excavating the nearby site of Trou des Nutons, a cave formed in the limestone hills of the Ardennes by the River Lesse, a tributary of the Meuse. Among the fossils found in the Trou des Nutons were beaver, roe deer, horse, bison and wild sheep, suggesting a later occupation than at Goyet. This was confirmed when another skull of a mystery ‘large canid’ was given a carbon date of 21,800 years BP. This is a surprisingly early date and in the middle of the last Ice Age. But was it the skull of a dog or a wolf?
These skulls from France were subjected to a series of precise measurements of snout-length and width, the length of the tooth row and the size of the flesh-shearing, self-sharpening carnassial teeth that wolves and dogs have where we have molars.
Fossil canid skulls from two archaeological sites in Russia and Ukraine, one at Mezin (Ukraine) and the other at Avdeevo just over the Russian border, were given the same treatment. These two sites were inhabited by early humans who constructed huts of mammoth bones and left behind an abundance of beads and other artefacts carved from mammoth ivory. The objective of the osteometric study of candid fossils from these two sites was to discover whether the remains of these ‘large canids’ differed sufficiently from wolves in their skull morphology to be classified as dogs on their way to domestication rather than unmodified wolves.
To complete the comparisons, the analysis was extended to include later, but still prehistoric, unambiguous fossil dogs from France and Germany. Also included were a selection of modern and fossil wolves from Europe and Asia along with modern dogs from several large breeds including Great Dane, Tibetan Mastiff, Siberian Husky, Chow Chow, Irish Wolfhound, Malinois, Dobermann Pinscher and German Shepherd.1
Comparing multiple skull measurements from dogs of different sizes is a complicated business, and I will spare you the details of the multivariate analysis and go straight to the main conclusion. The Palaeolithic skulls from the oldest sites, including Goyet at 31,700 years BP, had a significantly different shape from modern, or indeed fossil, wolves. This suggests that, even by that early date, these animals were dogs already on the way to modification through ‘domestication’. An alternative explanation, though in my opinion rather less likely, is that these were the skulls of one or more wolf species that later became extinct. As we shall see later, there is other enticing evidence to support the former scenario and suggest that the close association between wolf and man began a very long time ago.
The next layer of evidence about the changing appearance of domesticated dogs comes from the late glacial period around 17,000 years BP, when the ice sheets covering northern Europe were fast retreating. The shrinking tundra no longer supported herds of large prey animals. The climate warmed considerably, rainfall increased and forests covered much of the formerly open tundra. The fauna changed with the landscape and many prey animals disappeared. Mammoths, woolly rhinoceros and their predators, the sabre-tooth tiger and cave bear, were forced into extinction. Others, like the wild horse, reindeer and bison, shifted their ranges. Humans began to spread north, first following the shrinking herds and later, as they entered the Mesolithic period, changing their diet to smaller woodland prey, like wild boar, pine marten, red and roe deer. On the coastal settlements, shellfish became a major source of food and the first boats ventured out to sea to catch fish. Supplementing this meagre protein diet were roots and tubers, insects and snails. The heroics of the mammoth hunt became a thing of the past and life became a gruelling fight for survival.
The close cooperation between human and dogs, by now thoroughly assimilated into human society, continued even though the superbly effective working partnership that had developed in the Upper Palaeolithic was at its best when killing large prey, a practice which by now was rapidly disappearing.
Around 12,000 years BP much smaller dogs made their debut in the fossil record. A team of French archaeologists found the remains of thirty-nine dogs at the Pont d’Ambron rock-shelter in the Dordogne. From an osteometric analysis similar to that carried out at the earlier sites of Goyet and Trou des Nutons in the Ardennes, it was clear that the Pont d’Ambron dogs were considerably smaller. The same was true with the remains excavated at the Montespan cave in the northern foothills of the Pyrenees and at the open-air site of Le Closeau in an old channel of the River Seine.
The authors of the exhaustive paper summarising this body of work confidently concluded that they were dealing with the remains of dogs and not wolves. In France at least, and also in Spain, dogs were clearly changing. In Russia, however, at around the same time, wolf-dogs were still very large. Whether this was a result of separate wolf domestications in the two regions or for some other reason, it was impossible to say. One firm but rather grisly conclusion, drawn from cut-marks on the bones of the Pont d’Ambron dogs, was that they had been butchered and, presumably, cooked and eaten.
As well as the issue of timing, the identification of the geographical location of the wolf–dog transition has absorbed many researchers and continues to do so. The first scenario to be proposed, by a group from the University of Konstanz in Switzerland led by Peter Savolainen, was that the major ‘domestication’ event happened only once, in East Asia.2 This was the conclusion of an mDNA study of 654 dogs from different regions of the world where the focus was on the diversity of sequences. The perfectly sensible rationale was that the highest diversity, that is the highest number of different mDNA lineages, would be found in the places where dogs had been around the longest and had the most time to accumulate new mutations, rather like the islanders in our metaphorical example. Savolainen’s team found mDNA sequence diversity was highest in south-east Asia and located the first ‘domestication’ to the region. This was a very controversial conclusion at the time, and it would be another decade before the debate was settled, although it still rumbles on in some quarters.3
In order to make progress on the vexing issues of timing and location, scientists turned to the DNA that had, incredibly (a word I do not use lightly), survived in fossils. Robert Wayne, who headed the Los Angeles lab, was one of the eclectic bunch of scientists who dared to think, against all reason and common sense, that DNA might survive in fossils. As there was no academic tradition of ancient DNA science and this was an entirely new field, the early pioneers came from all sorts of backgrounds. Svante Pääbo, for example, who went on to sequence Neanderthal DNA, was originally an immunologist with an interest in Egyptology that led him to attempt to extract DNA from mummies in 1985. Ed Golenberg, who claimed in a 1990 Nature article that he had extracted DNA from a 17-million-year-old magnolia leaf, was a botanist. Scott Woodward, in a paper published by Science in 1994, reported DNA extraction from a fossil dinosaur Tyrannosaurus rex from the Cretaceous period entombed in a block of coal. Woodward was a geneticist from Brigham Young University in Utah who went on to run a large genetic genealogy project for the Mormon Church. My own background was in medical genetics, specifically the causes of inherited bone disease. In 1989 my colleagues and I reported the first recovery of ancient bone DNA in Nature.
We met regularly to feel our way in this exciting but tricky field where extravagant claims could be accepted for publication by the very best journals – and, more often than not, be rapidly dismissed. Robert Wayne was a regular attendee at these meetings. He is an evolutionary zoologist with an interest, at the time, in the hybridisation of wolves and coyotes where their ranges overlapped. Robert has gone on to become the pre-eminent scientist in dog genetics, first with work on fossil DNA and then with extensive analyses of the genetic variation in living dog breeds. Much of what we know about the genetics of dog evolution comes from Wayne’s lab in Los Angeles. I was slightly surprised to discover that Wayne doesn’t own a dog, but he does have a cat.
Once the field settled down in the years following the initial papers on ancient DNA recovery, a number of labs began to report its successful extraction from fossil wolves and unambiguous dogs, sometimes of great antiquity.
The field advanced in fits and starts, at first with the publication of single cases, then a few related finds and eventually, in 2013, a large series that seems, for now, to have settled the question of the origin of the wolf–dog transition in favour of Europe between 19,000 and 32,000 years ago.4
In the first decade of this century, the protocols for recovering ancient DNA improved a great deal and it became realistic routinely to obtain long sequences from old bone. Once again mitochondrial DNA was the target, for the very good reason that there are far more copies in a cell compared to nuclear DNA. If you are working at the limits, as you always are with ancient DNA, you want to make things as easy for yourself as possible.
DNA sequencing technology had also advanced to a point where it became practicable to sequence all 16,727 bases of the canid mitochondrial genome from fossils. Analysing the complete sequence avoided the potential bias of restricting the analysis to the shorter ‘control region’ used in the earlier papers by Wayne and Vilà and by Savolainen. The large 2013 study used more or less complete mitochondrial sequences of eighteen fossil ‘canids’ along with a large collection of modern dog breeds. Although not every specimen yielded all base pairs of sequences, it was enough to place them accurately on the evolutionary tree. Nuclear DNA, conversely, was too badly preserved to be of much use.
The resulting tree, or phylogram, to use the proper name, again recognised the four main branches (I–IV in the figure on page 17) of modern dog breeds initially published by Wayne and Vilà. The results were fascinating. The fossil dogs on three of the four branches (I, III, IV) of the tree are closely related to modern breeds while the rare fourth, mainly Scandinavian, branch (II) is closest to modern wolves from Sweden and Ukraine. One possible explanation is that dogs on this branch, which include the Norwegian Elkhound and the Jämthund, acquired their mitochondrial DNA from wild wolves in the recent past, after the advent of agriculture.
While all of the ancient dog lineages have survived to the present day, that is not the case for the fossil wolves. Many of these lineages are now extinct or have simply not been picked up in living wolves yet, though the likelihood of that diminishes as more and more modern wolves are sequenced.
There is a wealth of fascinating detail in the 2013 paper by Olaf Thalmann, which I encourage you contemplate at your leisure from the original publication.5 I do, however, want to mention one particularly surprising finding – about dogs in America. Only two fossil dogs were sequenced, one from Argentina and the other from Illinois, USA. From these mitochondrial sequences these dogs were clearly both related to branch I European dogs, though the ages of the fossils (1,000 and 8,500 years BP respectively) mean that they must have arrived well before the first European settlement in the fifteenth century. These dogs accompanied the indigenous Native Americans who had arrived earlier from Asia. None, however, had mitochondrial DNA remotely like that from American wolves. This has to mean that Native American dogs were ultimately descended from European and not American wolves.
There was another surprise in store. Breeds thought to have been descended from indigenous ‘Pre-Columbian’ dogs, like the Chihuahua and Mexican Hairless, also had an exclusively European mitochondrial heritage. Although sample numbers are quite low, it does look as if the indigenous Native American mitochondrial lineages were another casualty of European settlement.
As the dust settles on the controversies still hovering over the timing and location of the transition from wolf to dog, one thing is certain. It all began a very long time ago.