The Wolf Within: The Astonishing Evolution of the Wolf into Man’s Best Friend

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 here) 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.

7

The Cave of Forgotten Dreams

Though hardly fixing the dawn of the transition between wolf and dog with any degree of precision, the genetic dates are embedded in the bounds of what we call the Upper Palaeolithic – the last of the three phases of the Old Stone Age.

The origin of this classification, which is still used today, can be traced to John Lubbock, 1st Baron Avebury. A banker by profession, he also had a wide range of other interests including politics, biology and archaeology. His interest in the natural world grew from his friendship with Charles Darwin, who moved to the same village, Downe, in Kent, in 1842 when Lubbock was eight years old. As Lubbock matured, his interest in evolution and archaeology grew. He became an ardent supporter of Darwin’s evolutionary theories and of academic liberalism in general. He bought land in Wiltshire to save the famous prehistoric stone circle at Avebury from destruction and introduced into Parliament a bill that would eventually become the Ancient Monuments Act, the forerunner of all legislation to protect ancient sites.

Lubbock divided the Stone Age into two phases, the Palaeolithic, sometimes known as the Old Stone Age, lasting until roughly 10,000 years ago, and the Neolithic, the New Stone Age which followed it, coinciding with the invention of agriculture. Later an intermediate phase, the Mesolithic or Middle Stone Age, was adopted as the term for the period between the end of the last Ice Age about 17,000 years BP and the dawn of agriculture when the Neolithic began. About 4,000 years ago, the Neolithic gave way to the Bronze and then Iron Ages. The Palaeolithic was further divided into Lower, Middle and Upper phases, with the last of these lasting from about 50,000 years BP until the transition to the Mesolithic. Incidentally, the dates here only apply to the Stone Age in Europe. In other parts of the world the transitions occurred more recently; indeed, in highland New Guinea the Stone Age lasted until well into the twentieth century.

The genetic dating places the wolf–dog transition firmly within the Upper Palaeolithic, a quite extraordinary period in the history of our species, bristling with innovation and new ideas. The hallmark of the Upper Palaeolithic is the appearance of new forms of stone tools, the most durable of evidence. Until then, the only tools were hand axes and spear points. They were carefully made, certainly, but had not changed in basic design for tens of thousands of years. Suddenly, archaeologists were finding delicate arrow points, bone needles, even fish hooks, artefacts never seen in older, deeper layers.

Human fossils were much scarcer than stone tools, but they too showed a change from heavy-boned and robust skeletons whose skulls boasted prominent brow-ridges and receding chins to an altogether lighter and more graceful form. Was this a change brought about by slow adaptation, or was it the sign of the arrival in Europe of a new human species? After years of debate the argument was settled in favour of the wholesale replacement of the indigenous humans – Homo neanderthalensis, the Neanderthals – by a new arrival from Africa. This was Homo sapiens, our own ancestors. Mitochondrial genetics was the deciding factor in settling the argument in favour of replacement.

A few days before Christmas 1994 three speliologists, Eliette Brunel-Deschamps, Christian Heller and Jean-Marie Chauvet, were clambering over the face of the Ardèche gorge in southern France. Here the river cuts through the southern flanks of the limestone Massif Central on its way to join the Rhône near St-Just, well on its way to the Mediterranean. It is in the nature of limestone to form underground cave systems when exposed to the constant attention of slightly acidic groundwater. Over thousands of years the water gradually erodes the rock, hollowing out caverns of sometimes immense proportions.

The entrances to some 4,000 caves, many little more than overhangs, some as vast as medieval cathedrals, punctuate the steep walls of the gorge. Most are clearly visible, while others are hidden by rock-falls and vegetation. It was in order to find these hidden caverns that Jean-Marie Chauvet and his companions were inching their way along the steep sides of the gorge. They were searching for air currents emerging through cracks and crevices that would betray the presence of a cave system deep underground. At one point Chauvet felt a slight breeze coming from the rocks brushing the hairs on the back of his hands. He bent down to sniff the subterranean zephyr, then called his companions over. They agreed that the gentle flow smelled promisingly, damp, ancient and strangely alive. One by one they carefully removed the small rocks surrounding the vent until they came to a narrow cleft through which the air was escaping. It was too narrow for any of them to squeeze through, so next day they returned with hammers and a small pneumatic drill and set to work widening the crack. They found themselves faced with a narrow shaft descending into the black depths. Being experienced, not to say fearless, potholers they squeezed through the gap until they reached a point where a gallery opened out in front of them. It was clear, only from inside, that the main cave entrance had been blocked by an ancient rock-fall and that they had somehow found their way into the main cavern through the roof.*

As they explored the cave system over the following days the true wonder of their discovery began to dawn on them. Gleaming stalagmites rose up from the cave floor to meet their counterparts, delicate stalactites, suspended from the roof. Formed by the steady drip-drip-drip of calcium-rich water, their pristine condition showed that no animal or human had disturbed these hidden depths for thousands of years. On the floor lay scattered bones and skulls of cave bears petrified beneath a glassy coating of calcite.

This image actually comes from an exact replica of Chauvet cave that opened in Vallon-Pont-d’Arc in 2012, as access to the ancient caves is severely restricted for the protection of the artwork. The replica art was created using the same tools and methods as it is believed were used by the original artists. (Getty/AFP/Staff)

As Chauvet and his companions pushed further and further back along the galleries they saw in front of them the first of the paintings. Dozens of crude human hand prints outlined in red ochre covered one of the walls to a height of nearly two metres. These were only an introduction to the treasures which lay further back. There, on the deliberately smoothed cave walls, were drawn the images of lions, bears, mammoths, rhinoceros, horses and giant deer. These are the oldest morphologically accurate depictions anywhere in the world. What strikes home about them is their beauty. These are not merely crude outlines like the hand prints in the antechamber. They have form, expression and movement.

A painting from Chauvet cave that shows the head and horns of two aurochs, an extinct form of wild cattle that would have been a key prey animal for both humans and wolves. (JAVIER TRUEBA/MSF/SCIENCE PHOTO LIBRARY)

As well as being objects of wonder in themselves, these paintings have naturally led us to contemplate the reason they were drawn in the first place. What a task it must have been. Working deep underground without any natural light, the artists, for that is what they were, could only illuminate their lithic canvases by the light of glowing wooden torches. Streaks on the walls show where they had rubbed the dying embers to rejuvenate the flames. Carbon-dating the charcoal smeared on the walls was the means of discovering how long ago the drawings were made.

All organic material contains carbon, and this can exist in two forms called isotopes. Carbon 14 is very slightly radioactive. The other isotope, carbon 12, is not. After an animal or plant dies, or is burned in the case of the wooden torches, the radioactive carbon 14 slowly decays with a half-life of almost 5,000 years. In other words after 5,000 years there is only half as much carbon 14 remaining. By comparing the content of the two isotopes using a mass spectrometer to count the atoms, the age of the specimen can be estimated. Atmospheric carbon 14 is generated by ionising radiation from the sun high up in the atmosphere, some 32 kilometres above the ground. The proportions of the two carbon isotopes in the atmosphere are more or less in equilibrium. Thus the ratio of the carbon isotopes in a freshly dead animal or plant is equal to the atmospheric ratio at the time.

There are many factors that can change this ratio artificially and consequently introduce errors in dating. One is contamination of old material with modern carbon, for example from the archaeologists who recovered the specimen. This tends to make the material appear younger than it actually is. As is well known, carbon dioxide levels in the atmosphere have rocketed due to human activity since the Industrial Revolution. This carbon is ancient, coming as it does from the burning of fossil fuels that are millions of years old and no longer radioactive. This tends to reduce the carbon 14 in a specimen and artificially increase its apparent age. Nuclear testing also affects atmospheric carbon but in the opposite direction. Enormous amounts of carbon 14 are released into the atmosphere by a nuclear explosion, which in turn reduces the time estimate for radio-carbon dating. Nowadays these influences are incorporated into the calculations and the dates produced are referred to as ‘calibrated’. The original pioneers of radiocarbon dating did not take these influences sufficiently into consideration, and as a result many of the dates claimed in the earlier days of carbon-dating are wrong.

Thankfully, Chauvet cave was not discovered until the modern era of calibrated radiocarbon dating, and the dates obtained from the charcoal and other organic material in the caves can be relied upon. They show that Chauvet cave has been used for at least 80,000 years, first by cave bears, the skulls and bones of which litter the cave floor, then by an assortment of more recent Upper Palaeolithic mammals including hyenas and a couple of wolves.

There appear to have been two distinct phases of human ‘occupation’. The first was between 37,000 and 33,000 years ago and most of the drawings date to this phase. A later phase of occupation which produced the crude hand prints outlined in red ochre lasted from 31,000 to 28,000 years ago.

Chauvet cave is one of a handful of decorated caves from this remarkable and crucial phase in human evolution, the others being Lascaux in the Dordogne region of south-west France and Altamira in Calabria, northern Spain. Unlike the other two, Chauvet is in pristine condition, never having been open to any but bona fide researchers under strict instructions not to disturb the cave in any way. Altamira and Lascaux were open to the public for many years before the damaging effects of exhaled moisture and carbon were fully appreciated. They are now effectively closed to prevent further damage, though visitors can enjoy the visual impact of the caves and their paintings in nearby reconstructions.

In many people’s opinion the Upper Palaeolithic warrants comparison with other transformational periods in human cultural history: the rise of democracy in ancient Greece, the Italian Renaissance, the Age of Reason. So many new things were happening to the way we lived and most importantly to our interactions with the world around us. Many of these developments remain unseen and only reveal themselves in very special circumstances. Such a one is the discovery of Chauvet cave. There must be other caverns like it still sealed inside their limestone tombs, waiting for their breath to percolate to the outside. These caves give us rare glimpses into a vanished world, so very different from our own. Yet we see from the drawings that in many ways the artists were very much like ourselves. We understand the murals. Without difficulty we sense their beauty.

There are no human remains in Chauvet cave and, other than the drawings, very little sign of human presence. Nobody lived in Chauvet. What then was the purpose of these drawings, made with such effort and such skill? Clearly they were not purely decorative in the way we might hang a favourite painting on the wall above the fireplace. Although we will never know for certain, to many eyes these beautiful drawings are a tangible expression of a world of imagination and spirituality that marked the rise of truly modern humans.

An aspiration to go beyond what is absolutely necessary for function is also apparent in the stone tools our ancestors left behind. Whereas Neanderthals made perfectly functional tools like hand axes and thrusting spear points, they appear clumsy in comparison to the beautifully fashioned arrow points of the Upper Palaeolithic. The flint itself was traded over long distances and it supplied the raw material for individual craftsmen to demonstrate their skill. Fashioning a flint arrowhead or spear point was an opportunity not just to replace equipment lost in the hunt but also to demonstrate a high level of dexterity.

Quite suddenly, archaeological sites of the period were flooded with personal adornments. Excavations in south-west France reveal the appearance of bracelets, pendants and beads exquisitely fashioned from bone, antler and ivory. Seashells from the Mediterranean are found in sites hundreds of kilometres from the coast. Splinters of stone called burins were used to drill out holes in animal skins so that they could be sewn together with sinews for clothing. The effort involved was substantial.

Further afield at Sungir, 200 kilometres to the east of Moscow, archaeologists have excavated five human burials dated to 32,000 years BP, one of which contains the remains of a boy almost covered in strands of beads. There were nearly 5,000 beads in all, each one taking an estimated forty-five minutes to an hour to produce, a total of at least 4,000 hours in the making. On his head he wore a cap decorated with more beads as well as the canine teeth of at least sixty Arctic foxes. This was evidently the resting place of someone from an important family, a clear sign of social stratification emerging very soon after our ancestors arrived in Europe.

Our impression of our Stone Age ancestors is one of brutish simpletons clinging on in the face of appalling odds, surrounded by vicious and hungry predators looking for an easy meal. Certainly, their world was full of danger and life was hard. Nevertheless not every minute was taken up by the struggle to survive, and the evidence from Sungir shows that in some circumstances there was enough of a surplus for what we might imagine to be luxury, at least for a few. This was the world into which the wolf-dog was welcomed.

Far from being frightened prey cowering inside dank refuges, by the beginning of the Upper Palaeolithic our ancestors were well on the way to becoming top predators themselves. One by one the carnivores that once struck fear into the Neanderthals were driven to extinction. That perennial whipping boy of evolution, climate change, may have been the underlying influence behind the diminishing herds of mammoth and bison. But the climate had been changing for a very long time. Only when our ancestors arrived on the scene around 40,000 to 50,000 years ago did numbers of megafauna plummet. First the mammoth and the woolly rhinoceros vanished from the steppes, followed by the giant elk Megaloceros, then the bison and the wild horse. These were the herbivores that nourished the guild of carnivores and whose demise presaged their own extinction. The cave lion, leopard, hyena and sabre-toothed cat all vanished. The fearsome cave bear Ursus spelaeus who fought our ancestors for living space soon followed. Only the brown bear, Ursus arctos, managed to survive in the face of human competition by more or less abandoning meat altogether and restricting its diet to plants, berries and the occasional small mammal. At the end of the Palaeolithic all the large mammals, herbivores and carnivores alike, whose images jostled for space on the lime-smoothed walls of Chauvet, were gone.

A parallel wave of extinctions swept North America once humans arrived in numbers. As a species, we have never been good at taking responsibility for the damage we inflict, and the role humans played in the extinction of the North American megafauna is hotly debated. There is no doubt in my mind that both in Europe and in America it was our own human ancestors that pushed species after species over the edge into oblivion. In Europe none survived the hunting onslaught of our ancestors, but in North America, when the mammoth and the woolly rhinoceros went under, the elk and the buffalo survived.

Although technical invention in hunting equipment no doubt helped our ancestors to become the top predators, there was more to it than that. Certainly, the atlatl or spear-thrower was a deadly innovation which allowed our ancestors to kill at a distance and avoid injury, though alone it was hardly enough to account for the decimation of the megafauna. This piece of equipment was certainly one ingredient in our progress towards dominance of the Upper Palaeolithic world, but it seems unlikely that we achieved this distinction just because we could throw spears further and with more force than before. It was the revolution in our minds that took place all those years ago, as witnessed by the lavishly decorated burials of the children of Sungir and the gleaming frescoes of Chauvet, that really made the difference.

Artwork of how a spear-thrower (or atlatl) is used to throw a feathered dart. At top and centre, the dart is loaded. At bottom, it is being thrown. The angular momentum imparted means dart speeds of 150 kilometres per hour can be achieved, making this a lethal weapon in the hands of a skilled hunter. In the background is a cave painting of an animal wounded by an atlatl dart. The earliest such weapons were found at Schoningen, Germany, in the 1990s, dating to over 300,000 years ago. (KENNIS AND KENNIS/MSF/SCIENCE PHOTO LIBRARY)