Friday, March 30, 2018

Raised by Wolves

Michal Rovner: Night-7, 2016. Rovner’s work is on view in the exhibition ‘Evolution,’ at the Pace Gallery, Palo Alto, March 9–April 15, 2018.
One day around 26,000 years ago, an eight-to-ten-year-old child and a canine walked together into the rear of Chauvet Cave, in what is now France. Judging from their tracks, which can be traced for around 150 feet across the cave floor, their route took them past the magnificent art for which the cave is famous and into the Room of Skulls—a grotto where many cave-bear skulls can still be seen. They walked together companionably and deliberately, the child slipping once or twice, as well as stopping to clean a torch, in the process leaving a smear of charcoal.

It’s nice to imagine that the pair’s Huckleberry Finn–like exploration became the stuff of legend in their clan, for at the time Chauvet Cave’s recesses were abandoned, its art and cave-bear bones were already thousands of years old, and soon thereafter a landslide would seal the cave entrance. Whatever happened, the pair’s adventure certainly became famous in 2016, when a large radiocarbon dating program that included the smear of charcoal discarded by the child confirmed that the tracks constitute the oldest unequivocal evidence of a relationship between humans and canines.*

You might think that fossil bones and ancient DNA would allow scientists to trace our relationship with canines through the transition from wolf to dog, but this is not straightforward. Over thousands of years of domestication, canine DNA has become hopelessly mixed, and even the most complete Ice Age canine skeletons cannot be absolutely identified as wolf or dog. A 36,000-year-old canine skull from Goyet Cave in Belgium illustrates some of the problems confronting researchers. It is the earliest dog-like skull ever found, being relatively small and short-faced, as dogs’ are, but wolves’ generally are not; yet genetic analysis reveals that it is not closely related to any living wolves or dogs.

Genetic studies of wolves and dogs indicate that their lineages split between 30,000 and 40,000 years ago, and the limited archaeological evidence suggests that the split occurred in Europe. Cattle, sheep, goats, and pigs were all first domesticated much later—beginning around 10,500 years ago—in the Near East. The realization that humans and dogs have been companions for at least 30,000 years has prompted a reconsideration not only of the relationships’ origins, but also of its consequences.

In The First Domestication, Raymond Pierotti and Brandy Fogg argue that important insights into the origins of the canid–human relationship can be gained from studying the relationships between various indigenous peoples and wolves, which they claim are often ones of mutually profitable coexistence. One example concerns the Blackfoot people (NiiTsitapiiksi) of what is now Montana and parts of western Canada. They “were fond of wolves as companions,” sleeping on wolfskins and singing songs to encourage wolves to join them in a hunt. Numerous American indigenous cultures, it seems, have stories about wolves and humans sharing food and cooperating in other ways. The corpus of stories provides Pierotti and Fogg with evidence indicating “solid cooperation and a form of reciprocity…linked to guiding and the sharing of food.” Intriguingly, the stories often involve wolves helping women, and in Pierotti’s experience wolves and wolf/dog hybrids have a natural affinity for women that is only rarely seen when they interact with men.

Pierotti and Fogg believe that humans and wolves, both being large, intelligent social carnivores, were preadapted by evolution to cooperate with each other. As attractive as this idea is, it cannot be the whole story, for humans and social canids have coexisted for hundreds of thousands of years, yet there is no genetic or archaeological evidence of a bond forming until around 30,000 years ago. So we must ask ourselves why, if we are predisposed to bond, our species and African wild dogs, which coexisted for hundreds of thousands of years, did not form a bond; and also why Neanderthals and Denisovans, which coexisted with wolves for half a million years, likewise did not do so. And most intriguingly, why did modern man, who coexisted with wolves after humans left Africa 60,000 years ago, not form a bond until 30,000–40,000 years ago, after they entered Europe?

An important clue may exist in the nature of those first Europeans, for they were very unusual hybrid beings that resulted from the interbreeding of Neanderthals and humans. Until new migrations arrived in Europe 14,000 years ago, Europeans had a high proportion (around 8 percent) of Neanderthal genes, a figure that in modern populations is reduced to around 2 percent. As the well-documented phenomenon of hybrid vigor illustrates, hybrids can be highly distinctive, exhibiting characteristics seen in neither parent, and it is worth investigating the possibility that the Neanderthal/human hybrids interacted with canids in novel ways that led to domestication.

Conventionally, when we think of domestication, we envisage a process driven by humans and imposed on the creature being domesticated. But Pierotti and Fogg reframe it as an evolutionary process that was driven by cooperation and mutual benefit, and that profoundly shaped both species. They outline their concept in a hypothesis based on “thirty years of research experience watching wolves and their interactions with humans and with one another combined with careful studies of the traditions and attitudes towards nature of Indigenous peoples in North America.” The hypothesis begins with a subordinate, pregnant female wolf that decides to make her den adjacent to a human camp. A human female feeds her, and her cubs grow up with humans nearby, allowing the humans and wolves to learn how to cooperate.

This cooperative model of domestication is new, and it challenges the more conventional view that domestication was initiated by humans who took wolf cubs back to their camp, where they were fed and grew up in a human society. Given the scant archaeological record, either view could be correct, but what is really striking about Pierotti and Fogg’s hypothesis is the idea that once the relationship began, it proceeded as a form of coevolution that had a significant effect on human social structures. They even go so far as to write:
There are…indications that human social and even ethical systems—which many admire and hold, at least in theory, to be the highest achievement of humanity—were invented first by early canids.
In support of this idea they cite researchers arguing that “wolves had a powerful influence on the social ethics of early human groups through a kind of ‘lupification’ of human behavior.” These are startling and novel ideas, but without knowing more about the social structures of humans who lived without dogs (such as Tasmania’s Aborigines), it is difficult to assess how “lupified” we are relative to our ancestors before they associated with wolves.

One of the most persuasive of Pierotti and Fogg’s arguments is that the relationship between humans and dogs can be divided into two phases: the period between around 40,000 and 15,000 years ago, which left little trace in dog anatomy, and a subsequent, more intense phase that led to rapid changes in it. Our understanding of the early phase is shadowy because it involved mostly behavioral changes that have left little in the fossil record. The latter phase, however, is marked not only by the appearance of anatomically distinctive dogs but of burials of dogs with humans, which attest to the growing bond between the species. There is even some genetic evidence that around this time a second, independent domestication of wolves occurred in East Asia. With the domestication of cattle, sheep, goats, and crops, the human–dog relationship changed yet again, for diets became less rich in meat, and there were flocks to guard. Finally, around 4,000 years ago, human selection of dogs for various traits intensified, and the earliest breeds, including greyhound-like types, emerged.

The relationship between canids and humans continues to evolve, and today its most fraught aspect involves interactions between that most independent canid—the wolf—and rural people. Attitudes toward wolves are at their most extreme in the US, where some people of European descent are deeply hostile to wolves in a way that is disproportionate to their potential to cause physical or economic harm. Pierotti and Fogg blame this wolf-hatred on Christianity, which they claim demonized wolves because “the Christian Church decided that many humans were living too close to nonhumans on a respectful basis.” By way of proof, they claim that the greatest haters of wolves in America tend to have “strong religious backgrounds.”

Distinguishing a dog from a wolf is not always straightforward, and because several US states have laws prohibiting the keeping of wolves or wolf/dog hybrids, expert testimony is often called upon to determine whether an animal is a dog or wolf. Pierotti has been called as a witness eighteen times; having kept wolf/dog hybrids and studied both wolves and dogs extensively, his testimony is highly valued. In many cases, he has been able to demonstrate that the canid in question has no admixture of wolf genes. But as he points out, there is a larger question here, for the laws assume that wolves are more dangerous than dogs, when in fact the reverse is true. In the US between 1979 and 1996, more than three hundred people were killed by 406 dogs, and only fifteen of these instances involved purported wolf/dog crosses, some of which, according to Pierotti, are “highly questionable.” The situation with purebred wolves is even more clear-cut, for there is not a single example of a wolf in nature killing a human in the entire history of North America.

It is alarming, although perhaps predictable, that in the US attitudes toward wolves are becoming divided along political lines, with Republicans continuing to introduce and support laws that restrict or persecute them, while First Nations people and many Democrats are much more tolerant, or even encouraging, of the animals. In Europe, by contrast, a more easygoing relationship is being established, as was demonstrated in 2016 when one of the first wolves to enter the Netherlands in centuries crossed the border from Germany. It wandered the streets of a village for several days, the sanguine Dutch displaying little more than minor concern. Elsewhere in Europe, however, where wolves cause more harm to livestock, schemes are in place whereby farmers are compensated by the EU for losses to their flocks. Conflict between wolves and humans in Europe will doubtless continue, but in Europe wolves have a bright future, in part because most landowners seem willing to abide by laws and regulations formulated to address their interactions with the animals. In the US, however, wolves continue to be shot whenever they encroach onto private land. As a result, today more wolves can be found in Europe than in all the US, including Alaska, despite the fact that Europe’s human population is more than twice as large as that of the US.

Profound insights into how dogs evolved from wolves come from a remarkable, multidecade experiment on foxes that was carried out under the supervision of the Russian geneticist Dmitri Belyaev from the 1950s onward. Because much of the research was published in Russian, How to Tame a Fox, which is cowritten by Lyudmila Trut—a central figure in the project over many decades—will be widely welcomed for the extraordinary detail it contains. Initiated at a time when Soviet science was suffering under the malign influence of Trofim Lysenko, whose false ideas on genetics and how to increase crop production found favor with Stalin, research of this type was extremely dangerous to conduct. Indeed, Dmitri Belyaev’s brother Nicholai, an acclaimed plant geneticist who was skeptical of and opposed Lysenko’s theories, was arrested and executed in 1937.
Pinacoteca Nazionale, Siena/Scala/Art Resource‘Saint Blaise commanding the wolf to give the pig back to the poor widow’; detail of a polyptych by Sano di Pietro, fifteenth century
This seems to have left Dmitri more determined than ever to see Russian genetics regain its international reputation for excellence. At first, he had to cloak his research as an attempt to increase production at fur farms; but after Lysenko fell from grace, and following Stalin’s death in 1953, he could work more freely. By the 1970s genetics was once again a respectable science in the Soviet Union, and geneticists in the West began to hear of Belyaev’s remarkable work. With international collaboration again possible, his astonishing results began to be independently verified.

Belyaev’s experimental method was simple in the extreme. Out of the thousands of silver foxes held at a fur farm, he simply selected for ones that were calmer than normal in the presence of humans. After just a few generations of selective breeding, some offspring of these slightly tamer foxes started to seek out human company. Breeding these individuals produced foxes that showed changes in their reproductive systems that are typical of domesticated animals, which often bear more than one litter per year. Astonishingly, a few of the selected foxes even began to wag their tails and bark—characteristics otherwise seen only in dogs. Eventually foxes were produced that had varied color patterns in their fur, curly tails, and floppy ears, all of which are characteristic of domesticated animals, but not wild ones. A few even began vocalizing with a sound that was reminiscent of human laughter. None of these traits had been selected for—Belyaev’s team selected only for a fox’s degree of comfort around humans.

Extensive checks, including experiments in which embryos from normal foxes were transplanted into the uteruses of selected females, were undertaken, in order to demonstrate that genes rather than learned cues were responsible for the changes. Despite the undoubted genetic basis of the change, the precise mechanisms remain poorly understood, though clearly hormonal regulation—particularly of stress hormones—is important. By demonstrating that a simple selection mechanism could, over an exceedingly brief time, have such a large effect, Belyaev’s experiment had a major impact on our understanding of how the dog–human relationship began.

In a Stone Age camp, humans would have had no control over adult canids. But if a few canids had lower levels of stress hormones and did not run away from humans in fear upon reaching adolescence, they may have formed a self-selecting group that developed a distinctive, human-associated ecology. As long as they remained genetically more or less isolated, domestication should have proceeded rapidly. The conundrum is thus why domestic dogs didn’t emerge earlier. Pierotti and Fogg posit one possible answer: they think that wolves, rather than domestic dogs, were better partners for Ice Age humans. With important new theories challenging orthodoxy, the origins and consequences of the dog–human relationship looks set to become a major topic of research.

The contemporary relationship between people and their dogs results from the long coevolution traced by Pierotti and Fogg, as well as genetic changes similar to those seen in Belyaev’s foxes. In some instances, the dog–human relationship can be deep—some would argue as deep as that between two humans. But do humans and dogs think in similar ways? Until recently the question seemed unanswerable. The American philosopher Thomas Nagel summed the situation up in his famous paper “What Is It Like to Be a Bat?,” in which he argued that the perceptions and experiences of bats and humans are so different that humans can never know the bat’s perspective, and vice versa. It’s an argument that’s been used to dismiss the idea that humans can know what it is like to be any animal species.

The advent of technologies like functional magnetic resonance imaging (fMRI) has created new ways to approach the question, and Gregory Berns, a neuroscientist with a deep love and respect for dogs, has spent his career using these new tools to understand how animals, and particularly dogs, think. The development of fMRI was a breakthrough because it potentially allows researchers to determine if the same structures are used for the same function in human and animal brains. As Berns puts it:
Where structure-function relationships in an animal’s brain are similar to those in our brains, it is likely that the animal is capable of having a similar subjective experience as we do. This, I believe, is the path toward understanding what it’s like to be a dog, or a cat, or potentially any animal.
The task Berns set himself turns out to be extremely challenging. Just getting dogs to enter and stay still in fMRI machines requires months of training, while fine-tuning the experiments to ensure that the results are genuine takes years. An important advancement came when Berns designed and conducted a definitive “marshmallow test” for dogs. The marshmallow test measures an individual’s ability to delay gratification. It was first conducted in the early 1970s on children as young as four, who were offered a choice of treats—one preferred and one less so. The experimenter would then leave the room and return in fifteen minutes with the preferred treat. At any time, however, the child could ring a bell, and the experimenter would return with the less preferred treat. In the 2000s brain scientists scanned the brains of the children (by then grown) who had taken the original test, revealing that those who had demonstrated an ability to delay gratification had increased activity in a part of the frontal lobe known as the inferior frontal gyrus.
The need for the dogs to remain motionless in the fMRI mach
ine limits the kinds of experiments that can be conducted, and as Berns began to construct his marshmallow test for dogs he experienced several false starts. He eventually settled on an approach that involved first training the dogs to understand that when they heard a whistle they would get a treat, and then training them to learn that, at a hand signal given by their trainer, they had to lie still in the fMRI even when they heard the whistle, after which they would get the treat. The tests turned out to be far more difficult to conduct than you might think. But after several modifications, the researchers became confident that they were testing the dog’s degree of self-control.

Scans of the brains of the dogs that passed the test showed that activity was focused in a small area of the frontal lobe—a location similar to that activated in humans who had passed the marshmallow test. That this specific behavior is associated with the same general area of the brain in humans and dogs, whose brains differ in many ways, was, Berns concluded, proof that we can know what it is like to be a dog—at least with respect to delayed gratification. Over the years, Berns and his colleagues have investigated many species and brain areas, and it is astonishing how very different species use similar areas of the brain for the same tasks. Nagel, Berns concludes, was wrong: we can know what it is like to be a bat, for “echolocation was just an amplification of perceptual skills that humans also possessed.”

The growing recognition that brain function in humans and animals can be similar is challenging the ways we interact with and use animals, and in order to investigate this Berns takes us back to an incident that occurred while he was in medical school. “Dog lab,” he says, “was supposed to demonstrate how various drugs affected cardiovascular function.” The students were divided into groups of four, each of which was presented with an anesthetized dog whose chest had been opened by a surgical assistant, so the students could observe its heart and lungs as various drugs were administered. At the end of the session, Berns severed the aorta of the dog his group was using, killing it instantly, because the alternative was watching the dog linger while an injection of potassium chloride killed it. Participation in the exercise is, Berns tells us, “one of the deep regrets of my life…. The lab didn’t make me a better doctor, and it diminished me as a human being.”

By way of summary, Berns writes, “With similar brain architectures for the experience of joy, pain, and even social bonds, we can assume that animals experience these things much like we do, albeit without the words for those subjective states.” Modern humans may need Berns’s science to convince us of the similarity between us and other animals, but I suspect that those Neanderthal/human hybrids who entered into a relationship with wolves tens of thousands of years ago already knew it.
  1. * Anita Quiles et al., “A High-Precision Chronological Model for the Decorated Upper Paleolithic Cave of Chauvet-Pont d’Arc, Ardèche, France,” Proceedings of the National Academy of Sciences, Vol. 113, No. 17 (April 26, 2016). 

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