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English setter

31 000 years ago huge glaciers still ruled the northern lands. Stone Age people wandered Europe in search of big game, making skillfully crafted weapons and paintings. In Goyet Cave, Belgium, some memories of this time can still be seen. Bones, midden piles and others signs of life accumulated to the back of the cave, where they have lasted until this day. A few years ago researchers found something interesting among the miscellaneous bones: the skull of a domestic dog.

Like other dog skulls, the Goyet skull resembles that of a young wolf. It has a shorter muzzle, proportionately longer lower jaw and somewhat smaller brains than an adult wolf does. However, the fully ossified skull bones show this animal was not a wolf cub. It was an adult dog.

It is not known how close the relationship between the Goyet dog and the people it lived with was. Was it a respected hunting companion that slept on the furs with its masters? Or was it a half-feral beast, stealing scraps of food, stalking at the edges of the camp, only tolerated because it’s bark would wake people up if cave lions attacked in the night?

It’s still the subject of much discussion where the dog originally came from, how and when was it domesticated. Just about the only thing everyone agrees on is that dogs are descended from wolves (Canis lupus).

The “where” has been suggested to be either in Middle East or Eastern Asia. The “when” varies even more wildly: from 16 000 years ago all the way to more than 100 000 years ago. Some DNA evidence suggests the wolf might have been domesticated multiple times, in different areas and times, to form the diversity of domestic dogs. It might well be that some instances of domestication did not leave any living descendants.

Modern dogs are friendlier, more curious and perhaps a bit less bright than their wild cousins. Above all, they have in a short time evolved an astonishing diversity of shapes and colours. How in Earth has all this happened? Perhaps surprisingly, some answers can be found not studying the dogs themselves, but foxes.

 Mr. Belyaev’s tame foxes

During 1950s a Russian geneticist named Dmitry Belyaev started a historical experiment. He bought 130 silver foxes (Vulpes vulpes) from Siberian fur farms and started breeding them for tameness. For each kit born in the facility, the researchers performed a simple test. A researcher would approach the cage, open it and touch the fox inside, while an assistant would write down how the kit reacted. Only the friendliest kits, those that showed least signs of aggression or fear, were then used to breed the next generation.

Initially, the purpose of the experiment was simply to help breeding more manageable foxes for fur farms. However, the results were so astonishing the whole project took a new turn. In just four generations, the first “elite foxes” were born. These were fully domesticated animals that showed no aggression or fear towards humans, instead wagging their tails and competing for attention. (photograph: Zefram/Wikipedia)


Longer windows

It seems that tameness in Belyaev’s fox kits was caused by longer duration of the socialization window and delayed onset of the fearfulness which is normal for adult foxes.

Socialization window is the time when a young canid will become sensitive to members of it’s own species, a process somewhat like imprinting in bird hatchlings. If there are members of other species around at this sensitive period, they will be included too.

In Belyaev’s foxes, this socialization window lengthened, and the same seems to have happened to domestic dogs. When a wolf pup is 2 to 3 weeks old, it’s socialization window is already closing. In dogs, however,  in only opens at the age of three weeks and stays so until the age of 12 to 16 weeks. This might be the most important component of domestication, since it gives much more time for the puppy to get to know humans in addition to it’s mother and littermates.

Young dogs, wolves and foxes are not usually afraid of new things or creatures, instead fearlessly exploring their surroundings. With age, they become less curious and more careful. In this aspect, too, domesticated foxes and dogs resemble each other more than their wild cousins.

Fearless exploring in wild wolf cubs and fox kits stops around the age of six weeks. Domesticated foxes and dogs, however, start maturing in this regard only at the age of 4 to 6 months, and they never become as careful as wild animals are.

domesticated and wild silver fox skulls vulpes vulpes maija karala

Spots and floppy ears

But Mr. Belyaev and colleagues were in for another surprise. Their brand new domestic foxes also started looking different.

Around the tenth generation of the experiment, some foxes started showing oddly dog-like traits: white and light brown spots on their fur, and shorter snouts and legs (domesticated (left) and wild (right) fox skulls above). Some foxes even had floppy ears or a tail curled over their backs. These characteristics were common in dogs, but virtually unheard of in foxes.

Because seeing is believing, here are links to some pictures of the domesticated foxes: black-and-white fox on Nature Library and a floppy eared one from redhotrussia.com.

Could it be that fur color and body shape were somehow genetically correlated with tameness? The researchers meticulously excluded all other explanations. They had been careful not to favour animals based on their looks. They had also a population of control foxes that had been treated and bred identically except for the domestication selection. In them, spots and floppy ears were extremely rare, as expected.

The Russian scientists suggest domestication brings a set of changes in appearance with it, regardless if they are favoured or not. Though they often are, since humans tend to favour animals that look different. These changes are common to many domesticated animals from horses to chickens, and were already noticed by Charles Darwin in The origin of Species, published in 1859. Darwin, however, had no idea what caused the phenomenom. Scientist are only today starting to figure out the answers.

Much like friendliness, curiousity and fearlessness, short legs and snouts are also characteristics of young animals. Very young cubs and kits have floppy ears, and on floppy eared individuals, they simply never spring up. As if the animals never grew up.

It just might be that there are no separate genes for “tameness”. Instead, domestication affects the genes that regulate maturing, and thus affects everything from body proportions to hormonal cycles. This retention of juvenile traits by adults is called neoteny. Neoteny (or, a bit more broadly, paedomorphosis) occurs in many groups of animals, but the domestic dog is a textbook example. The more extreme toy dog breeds actually resemble fetal wolves. Comparing the level of neoteny may give us new understanding about health problems or behavioural differences between dog breeds. (In the picture below, from top to bottom, the skulls of a wolf, a Siberian Husky, a Lhasa Apso and a Pekingese)

koirakallot pysty

White is childish

satu spanish water dog maija karalaEven the white blotches in Mr. Belyaev’s foxes and many dog breeds may be caused by neoteny. During fetal development, the pigment cells producing fur color arise from the neural crest, the same longish blob of cells that later develops into most of the nervous system. The pigment cells are supposed to migrate from the neural crest to the skin, where they attach to hair follicles and start producing pigments. White blotches may form if the neural crest develops too slowly and there isn’t enough time for the pigment cells to complete their migration.

Belyaev’s practical little experiment turned into a huge multi-decade project and is still running today. At times, it has been unpopular in the eyes of Russian leaders (as behaviour determined by genes didn’t fit the communist worldview) and still suffers from insufficient funding. As the facility cannot keep all the foxes they breed, they have had to sell them to fur farms, a traumatizing experience for both the animals and staff. Recently, however, the Russian scientists have finally gotten a permit to sell their tame foxes abroad as pets.

While writing this, a domesticated wolf, the descendant of ferocious predators and the result of thousands of years of careful breeding, insists I must either play with her tennis ball or hold all the 30 kilograms of her on my lap. That, if anything, is neoteny.

Edit 18.1.2013: I was kindly corrected that the picture originally linked of a fox with light brown blotches was in fact not a domesticated fox, but a North American cross fox, a color variety occurring in the wild.

References and further reading:

D. Darwin (1859) On the Origin of Species. London: John Murray.

D. Goodwin, J. W. S. Bradshaw & S. M. Wickens (1997) Paedomorphosis affects agonistic visual signals of domestic dogs. Animal Behaviour 53: 297-304.

A. Ruvinsky & J. Sampson (2001) The Genetics of the Dog. CABI.

L. N. Trut, I. Z. Plyusnina & I. N. Oskina (2004) An experiment on fox domestication and debatable issues of evolution of the dog. Russian Journal of Genetics 40(6): 644-655.

M. A. R. Udell, N. R. Dorey & C. D. L. Wynne (2010) What did domestication do to dogs? A new account of dogs’ sensitivity to human actions. Biological Reviews 85(2): 327-345.

The Retriever, Dog & Wildlife Blog: Another look at the Goyet Cave “dog”.

Wikipedia: Domesticated silver fox.

Scientific American: Man’s new best friend? A forgotten Russian experiment in fox domestication.

The Thoughtful Animal: Monday pets: the Russian fox story.

Slate: Guarding the fox house.

Red Hot Russia: The most affectionate foxes are bred in Novosibirsk. A lot of pictures!