This post is part of the series on Belyaev’s fox experiments.
(index | part I | part II | part III | part IV )

Animals, within the same species, can be truly varied.  Dog breeds, from Papillions to Greyhounds to Shiba Inus, are all the same species.  Belyaev commented: “Domestic animals differ from their wild ancestors, and from each other, much more than do some species and even genera.” This diversity is also seen within foxes, as there is a genetic difference between the ‘urban fox’ and the ‘rural fox’.  This is the same species, but they are significantly different because they have adapted to specific niches.

This difference was also seen between Belyaev’s selected-for-tameless line (‘the domesticated fox’) and unselected lines, as outlined below. These traits are still rare, however, with only ‘a few’ occurring out of every 1000-10000 individuals. These traits are not extraordinary, either, as these changes are typical of domestication in many other species.

 

Colour changes

Coat colour changes was the first change documented in the domesticated stock, in around the 8^th-10^th generation. Domesticated foxes are 1646% more likely to have depigmentation, 423% more likely to have brown mottling, and 400% more likely to have grey hairs, than their undomesticated cousins.  The colouration can be from patches of white on their foreheads, to spots of various colouration throughout their body, and piebaldness.

 

Floppy ears

Drop ears were observed around the 8^th-10^th generation.  Domesticated foxes are 35% more likely to have floppy ears than unselected farm foxes.

 

Tail changes

Tails changed position around the 8^th-10^th generation, with tails ‘rolled’ over the back.  Shorter tails were also observed, but at a later generation, approximately 15-20 generations into the experiment.  Domesticated foxes are 6900% more likely to have a short tail, and 1033% more likely to have a rolled tail than undomesticated farm foxes.

 

Reproductive Changes

Domesticated foxes reach sexual maturity earlier, give birth to larger litters, have a longer mating season than their unselected cousins.  However, there has not been any pups successfully reared to adulthood from an extaseasonal mating.  Many times the mating do not take and, when they do, the mothers are often cannibalistic.

 

Skulls and teeth

The domesticated foxes have smaller cranial height and width, and shorter/wider snouts than unselected farmed foxes.  Males also have a more feminine head (i.e. there is no clear difference between the sexes in terms of their head shape anymore).  Skulls in the domesticated fox are unusually broad for their length.

In regards to teeth, the domesticated foxes have smaller teeth than the unselected farm foxes.  After the 15^th to 20^th generation, underbites and overbites became apparent.

 

Hormonal changes

There are number of hormonal differences found in domesticated foxes, in comparison to the unselected foxes.  To put simply: Domesticated foxes have more serotonin (which is responsible for inhibiting aggression and generally ‘feeling good’).  This probably is responsible for the domesticated foxes having less ‘stress hormones’ in their system – because of the serotonin, they are less stressed.  As hormones have a rather complex and far-reaching role in development, it is probable that these results have implications across the animal.

The slightly more complex version of events:

Domesticated foxes have more serotonin, and more enzymes involved in the production of serotonin.  Serotonin is made by the liver and regulates mood, digestion, memory and learning, among other things.  In the foxes it is believed to inhibit aggression and development.

Corticosteroid levels, cortisol, and adrenocorticotpric hormone are all found in reduced levels in the domesticated fox.  These hormones come from the adrenal gland and the anterior pituitary gland in response to stress.  As these foxes are less stressed, they do not produce so much of these hormones.  Overall, domesticated foxes have less activity in their adrenal gland.  Additionally, the developmental spike in corticosteroid levels in domesticated foxes occurs much later than their undomesticated counterparts.

There are also changes in the level of steroid sex hormones, chiefly estradiol and progesterone in the domesticated foxes.  The role of progesterone in embryogenesis (development) is also significant.

 

Changes in the socialisation period

We know socialisation plays an important role for dogs, and it seems the same is the case in foxes. There is a ‘sensitive’ period of socialisation in post-natal development.

Is clear is that the domestication process in foxes has resulted in a different, extended socialisation period.  Firstly, they respond to sound two days earlier (and open their ears quicker) and open their eyes one day earlier (and also open their eyes quicker) than unselected foxes.  The socialisation period of the domedicated fox closes 3 weeks later than non-domesticated lines (i.e. the unselected foxes have a socialisation period of 40-45 days, while unselected foxes have a socialisation period of 60-65 days). Domesticated foxes have accelerated maturation intitially, and then this is retarded.  This means that foxes have an extended window, which allows them to learn more about human ways and how to respond to them.

Belyaev experimented with fox cubs from domesticated lines and lines selected from aggression.  From day 30 onwards, differences in the pups were clear.  Domesticated fox pups are more likely to move around in a new environment than aggressive lined fox pups.  But it is from day 40 that the most difference is seen.  Domesticated fox lines are less fearful, and more willing to overcome the fear in a new environment.  Aggressive lined pups were inclined to hide in a corner during the testing period – hunched, scared, and sometimes snarling.  This kind of fearful behaviour exacerbates difference between the lines, as fearful pups interact less with the environment and so have more foreign items to be afraid of in the future.

 

Other Difference

Domesticated foxes sound different (they sound ‘doglike’), they experience excitement urination, they have thinner bones, and moult in different ways to unselected stock.  Around the 15^th to 20^th generation, shorter legs were seen. Fox puppies from the domesticated line also respond to human cues (such as pointing) “as skilfully” as dog pups.

 

Pedomorphosis

Overall, these traits all fit into the descriptor of ‘pedomorphosis’.  This is the term to describe the retention of juvenile traits in adults.  This includes physical changes (in this example, the skull shape) to behavioural changes (such as whining and barking). As these foxes reach reproductive maturity despite the pedomorphosis, they are experiencing a form of pedomorphosis called neoteny.

The reasons for this neoteny, and related traits, will be examined in depth in Part III of my posts regarding Belyaev’s fox experiment.

 

An Illustration

My friend, Stefan Psarkos, made a physical model of the changes seen in Belyaev’s foxes. A photo of his model is shown below.  This model illustrates the depigmentation, floppy ears, and erect tail set that selection for tameness has been associated with.

 

 

References:

Belyaev, DK (1979). Destablizing selection as a factor in domestication Journal of Heredity, 70 (5), 301-308 [link]

Belyaev, D., Plyusnina, I., & Trut, L. (1985). Domestication in the silver fox (Vulpes fulvus Desm): Changes in physiological boundaries of the sensitive period of primary socialization Applied Animal Behaviour Science, 13 (4), 359-370 DOI: 10.1016/0168-1591(85)90015-2

Hare, B., Plyusnina, I., Ignacio, N., Schepina, O., Stepika, A., Wrangham, R., & Trut, L. (2005). Social Cognitive Evolution in Captive Foxes Is a Correlated By-Product of Experimental Domestication Current Biology, 15 (3), 226-230 DOI: 10.1016/j.cub.2005.01.040 [link]

Kukekova, AV, Acland, GM, Oskina, IN, Kharlamova, AV, Trut, LN, Chase, K, Lark, KG, Hollis, NE, & Aguirre, GD 2006, ‘The genetics of domesticated behavior in canids: What can dogs and silver foxes tell us about each other?’, The Dog and Its Genome, Cold Spring Harbor Labratory Press. [link]

“New Nice” on the Radiolab show in October 2009. [link] (I highly recommend this reference for a light hearted, audio version of this experiment.)

Trut, L. (1999). Early Canid Domestication: The Farm-Fox Experiment American Scientist, 87 (2) DOI: 10.1511/1999.2.160  [link](I highly recommend this reference for further reading.)

Trut LN. 2001. Experimental Studies of Early Canid Domestication. In The Genetics of the Dog (ed A Ruvinksy and J Sampson). CABI 2001, p.15-43.