Dogs Again

Having finally reached the topic of natural selection, we can turn back to the example of dogs for some other important lessons. I said that they are domesticated wolves, but I need to qualify this in the light of a fascinating theory of the evolution of the dog, which has again been most clearly articulated by Raymond Coppinger. The idea is that the evolution of the dog was not just a matter of artificial selection. It was at least as much a case of wolves adapting to the ways of man by natural selection. Much of the initial domestication of the dog was self- domestication, mediated by natural, not artificial, selection. Long before we got our hands on the chisels in the artificial selection toolbox, natural selection had already sculpted wolves into self-domesticated 'village dogs' without any human intervention. Only later did humans adopt these village dogs and transmogrify them, separately and comprehensively, into the rainbow spectrum of breeds that today grace (if grace is the word) Crufts and similar pageants of canine achievement and beauty (if beauty is the word).

Coppinger points out that when domestic animals break free and go feral for many generations, they usually revert to something close to their wild ancestor. We might expect feral dogs, therefore, to become rather wolf-like. But this doesn't happen. Instead, dogs left to go feral seem to become the ubiquitous 'village dogs' - 'pye-dogs' - that hang around human settlements all over the third world. This encourages Coppinger's belief that the dogs on which human breeders finally went to work were wolves no longer. They had already changed themselves into dogs: village dogs, pye-dogs, perhaps dingos.

Real wolves are pack hunters. Village dogs are scavengers that frequent middens and rubbish dumps. Wolves scavenge too, but they are not temperamentally suited to scavenging human rubbish because of their long 'flight distance'. If you see an animal feeding, you can measure its flight distance by seeing how close it will let you approach before fleeing. For any given species in any given situation, there will be an optimal flight distance, somewhere between too risky or foolhardy at the short end, and too flighty or risk-averse at the long end. Individuals that take off too late when danger threatens are more likely to be killed by that very danger. Less obviously, there is such a thing as taking off too soon. Individuals that are too flighty never get a square meal, because they run away at the first hint of danger on the horizon. It is easy for us to overlook the dangers of being too risk-averse. We are puzzled when we see zebras or antelopes calmly grazing in full view of lions, keeping no more than a wary eye on them. We are puzzled, because our own risk aversion (or that of our safari guide) keeps us firmly inside the Land Rover even though we have no reason to think there is a lion within miles. This is because we have nothing to set against our fear. We are going to get our square meals back at the safari lodge. Our wild ancestors would have had much more sympathy with the risk-taking zebras. Like the zebras, they had to balance the risk of being eaten against the risk of not eating. Sure, the lion might attack; but, depending on the size of your troop, the odds were that it would catch another member of it rather than you. And if you never ventured on to the feeding grounds, or down to the water hole, you'd die anyway, of hunger or thirst. It is the same lesson of economic trade-offs that we have already met, twice.*

The bottom line of that digression is that the wild wolf, like any other animal, will have an optimal flight distance, nicely poised - and potentially flexible - between too bold and too flighty. Natural selection will work on the flight distance, moving it one way or the other along the continuum if conditions change over evolutionary time. If a plenteous new food source in the form of village rubbish dumps enters the world of wolves, that is going to shift the optimum point towards the shorter end of the flight distance continuum, in the direction of reluctance to flee when enjoying this new bounty.

We can imagine wild wolves scavenging on a rubbish tip on the edge of a village. Most of them, fearful of men throwing stones and spears, have a very long flight distance. They sprint for the safety of the forest as soon as a human appears in the distance. But a few individuals, by genetic chance, happen to have a slightly shorter flight distance than the average. Their readiness to take slight risks - they are brave, shall we say, but not foolhardy - gains them more food than their more risk-averse rivals. As the generations go by, natural selection favours a shorter and shorter flight distance, until just before it reaches the point where the wolves really are endangered by stone-throwing humans. The optimum flight distance has shifted because of the newly available food source.

Something like this evolutionary shortening of the flight distance was, in Coppinger's view, the first step in the domestication of the dog, and it was achieved by natural selection, not artificial selection. Decreasing flight distance is a behavioural measure of what might be called increasing tameness. At this stage in the process, humans were not deliberately choosing the tamest individuals for breeding. At this early stage, the only interactions between humans and these incipient dogs were hostile. If wolves were becoming domesticated it was by self-domestication, not deliberate domestication by people. Deliberate domestication came later.

We can get an idea of how tameness, or anything else, can be sculpted - naturally or artificially - by looking at a fascinating experiment of modern times, on the domestication of Russian silver foxes for use in the fur trade. It is doubly interesting because of the lessons it teaches us, over and above what Darwin knew, about the domestication process, about the 'side-effects' of selective breeding, and about the resemblance, which Darwin well understood, between artificial and natural selection.

The silver fox is just a colour variant, valued for its beautiful fur, of the familiar red fox, Vulpes vulpes. The Russian geneticist Dimitri Belyaev was employed to run a fox fur farm in the 1950s. He was later sacked because his scientific genetics conflicted with the anti-scientific ideology of Lysenko, the charlatan biologist who managed to capture the ear of Stalin and so take over, and largely ruin, all of

Soviet genetics and agriculture for some twenty years. Belyaev retained his love of foxes, and of true Lysenko-free genetics, and he was later able to resume his studies of both, as director of an Institute of Genetics in Siberia.

Wild foxes are tricky to handle, and Belyaev set out deliberately to breed for tameness. Like any other animal or plant breeder of his time, his method was to exploit natural variation (no genetic engineering in those days) and choose, for breeding, those males and females that came closest to the ideal he was seeking. In selecting for tameness, Belyaev could have chosen, for breeding, those dogs and bitches that most appealed to him, or looked at him with the cutest facial expressions. That might well have had the desired effect on the tameness of future generations. More systematically than that, however, he used a measure that was pretty close to the 'flight distance' I just mentioned in connection with wild wolves, but adapted for cubs. Belyaev and his colleagues (and successors, for the experimental program continued after his death) subjected fox cubs to standardized tests in which an experimenter would offer a cub food by hand, while trying to stroke or fondle it. The cubs were classified into three classes. Class III cubs were those that fled from or bit the person. Class II cubs would allow themselves to be handled, but showed no positive responsiveness to the experimenters. Class I cubs, the tamest of all, positively approached the handlers, wagging their tails and whining. When the cubs grew up, the experimenters systematically bred only from this tamest class.

After a mere six generations of this selective breeding for tameness, the foxes had changed so much that the experimenters felt obliged to name a new category, the 'domesticated elite' class, which were 'eager to establish human contact, whimpering to attract attention and sniffing and licking experimenters like dogs'. At the beginning of the experiment, none of the foxes were in the elite class. After ten generations of breeding for tameness, 18 per cent were 'elite'; after twenty generations, 35 per cent; and after thirty to thirty-five generations, 'domesticated elite' individuals constituted between 70 and 80 per cent of the experimental population.

Such results are perhaps not too surprising, except for the astonishing magnitude and speed of the effect. Thirty-five generations would pass unnoticed on the geological timescale. Even more interesting, however, were the unexpected side-effects of the selective breeding for tameness. These were truly fascinating and genuinely unforeseen. Darwin, the dog-lover, would have been entranced. The tame foxes not only behaved like domestic dogs, they looked like them. They lost their foxy pelage and became piebald black and white, like Welsh collies. Their foxy prick ears were replaced by doggy floppy ears. Their tails turned up at the end like a dog's, rather than down like a fox's brush. The females came on heat every six months like a bitch, instead of every year like a vixen. According to Belyaev, they even sounded like dogs.

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