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A now-famous experiment in Russia had anticipated the same conclusion as the US team about the mechanism of domestication, but without the fearsome armoury of modern genetics. The experiment was noteworthy on its own, but perhaps even more remarkable was the fact that it was carried out at all. The scientist Dmitri Belyaev began working when Stalin’s regime was at its height. Stalin had appointed a Ukrainian, Trofim Lysenko, the son of a peasant, to dramatically increase Soviet agricultural production following the widespread crop failures that followed the collectivisation of farming in the early 1930s. Lysenko had an idiosyncratic approach to his task that rejected established genetic theory, believing instead that genes were unimportant in determining crop or milk yields. He insisted that improvements could be made only by altering the way in which animals or plants were treated. In the balancing act between nature and nurture, nature was ignored altogether. As Lysenko grew in prominence and influence, many of his opponents were removed from their positions, imprisoned or even executed. Genetics became a dirty word in Soviet Russia, textbooks were removed from university libraries and geneticists themselves became enemies of the State.
It was under these unpromising, to say the least, political conditions that Belyaev began. He worked in Moscow on a dissertation incautiously entitled ‘The variation and inheritance of silver-coloured fur in Silver-Black foxes’. Belyaev survived Stalin’s regime and in 1959 moved east to the Siberian town of Novosibirsk where he remained for the rest of his working life.
Soon after he arrived at his new laboratory he began his most famous breeding experiment, which he was able to disguise as a purely commercial exercise and thus avoid the long reach of Lysenko and his cronies. Silver foxes had been reared on Russian fur farms since the nineteenth century and fetched a good price. They are called silver foxes because of the white guard hairs which protrude beyond their otherwise blue-black coats, but they are in fact a colour variant of the familiar and widespread red fox Vulpes vulpes. Belyaev disguised his research as being designed to increase the proportion of silver guard hairs and thereby put up the value of the pelt. He began his selective breeding programme with that declared aim, but it was, in reality, purely Darwinian in design.
Instead of choosing to breed from foxes on the basis of their coat-colour, he chose a completely different criterion. He would select not on the basis of a physical characteristic at all, but instead on a single variation in behaviour, namely tameness. He began with thirty males and a hundred females from a commercial colony in Estonia where the animals had been bred for fifty years without selection of any kind. Belyaev was focusing on the foxes’ reaction to humans. They were still wild animals at heart, even though their ancestors had been in captivity for so long. Most of them reacted to humans with a mixture of fear and aggression, retreating to the back of their cages whenever approached and biting when anyone attempted to handle them. As you would expect, there was a variation between individuals from the colony, and about 10 per cent of them were noticeably more tolerant. The stage was set and the experiment began.
When the cubs were about four months old, Belyaev or one of his assistants would try to stroke them. This was repeated for the next three months. Belyaev chose the least aggressive animals to breed from, and these formed his experimental group. He was careful also to have a control group in which mating was random. After only twenty generations of selection the experimental foxes were showing consistent changes in their behaviour. They became affectionate towards humans almost as soon as they opened their eyes. They became playful and enjoyed the interaction with their keepers in ways that would have been unimaginable at the start of the experiment only twenty generations before. The extent of the behavioural transformation was remarkable, but less so than the speed at which it had occurred. Evolution under natural selection is an excruciatingly slow process, taking thousands or even millions of years to produce substantial changes of the magnitude shown by the foxes in only a fraction of the time. There were other surprises.
Dmitri Belyaev with his selectively bred foxes. Photographed in Novosibirsk, Russia, in 1984. (SPUTNIK/SCIENCE PHOTO LIBRARY)
Even though the criterion for selection had been entirely behavioural, after a while the experimental group of foxes began to exhibit physical changes. Their ears became floppy, their tails curled and their coats became uneven, with patches of different colours. The skull shape changed too, becoming broader and with a shorter snout, both features usually confined to immature animals and oddly reminiscent of the differences between wolf and dog.
Brian Hare, the expert on animal cognition, wanted to see whether these collateral changes associated with domestication extended to the ability to read human gestures. One summer he and his research associate visited the Novosibirsk facility and put the experimental foxes through their paces. He used the familiar baited cup trial and was astounded to find that the experimental foxes were absolutely brilliant at it, scoring far higher than by chance alone. It was hard to design the experiment to test the control group because the foxes were so skittish. Through a series of ruses, they were persuaded to perform, which they did rather badly. Along with the behavioural changes easily attributable to the single selection criterion, tameness, it seemed as if the assimilation process brought with it a genetic package that included some physical changes and cognitive abilities that we can easily distinguish in the domesticated dog.
The inference to be drawn from Belyaev’s work is that some of the physical changes associated with domestication do not have a direct genetic basis but are the effects of secondary hormonal adaptations following on from the selection for tameness.
Even though Belyaev’s research was carried out on foxes, the results may help explain the biological mechanism behind the human–dog bond. In 2015 a Japanese research group found evidence for the involvement of the hormone oxytocin in promoting the bond between the two species based on mutually understandable communication. Oxytocin has been called ‘the love hormone’ because its action serves to promote feelings of attraction and attachment between individuals. This appears to be a secondary effect of the hormone, whose principal activity is to dilate the cervix during childbirth.
Oxytocin is a short neuropeptide of only nine minor acids and is made in the hypothalamus deep in the brain behind the eyes. In a display of thrifty evolution, oxytocin orchestrates an impressive repertoire of different activities surrounding sexual reproduction, the close attachment we call ‘love’ being one of them.
All mammals use oxytocin for much the same reasons, but because human babies develop so slowly compared to other animals and are dependent on their parents, and particularly their mothers, for many years, the ‘bonding’ effects of oxytocin are especially strong.
It was always assumed the feelings of attraction and attachment induced by oxytocin only applied to members of the same species. However, in 2015 the Japanese scientists published a startling paper contradicting this long-held assumption by showing that oxytocin is closely involved in the strong bond that humans have developed towards their dogs – and vice versa.1
The scientists measured the oxytocin levels in thirty owners and their dogs, before and after they engaged in what was described as ‘mutual gazing’. It has been known for a long time that looking closely into each other’s eyes is a key factor in establishing the strong attachment of a mother and her baby. The Japanese study was the first to show that the same hormonal mechanism, involving oxytocin, is also behind the attachment of a dog and its owner. Levels of oxytocin went up after a session of mutual gazing, not just in the owners but in the dogs as well.
The same responses did not occur in encounters between humans and captive wolves, even those that are accustomed to close human contact. It seems likely therefore that the strength of the human–dog bond, mediated through oxytocin, is a direct consequence of the selection process that turned wolves into dogs.
Oxytocin itself has been used in the treatment of autism and of post-traumatic stress disorder, and it may well be the case, though this is yet to be proven, that therein lie the benefits of assistance dogs for these and other conditions. The finding that dogs also experience an oxytocin surge after mutual gazing suggests that the ‘love’ is reciprocated rather than being a ploy on their part to bring out favourable behaviour in ourselves.
Belyaev died in 1985, but his long-time associate Lyudmila Trut has carried on the experiment, which is partly financed by the sale of her remarkably affectionate foxes as pets.