Repost: Learning from Domesticated Foxes

[This was originally a guest post on The Thoughtful Animal.]

Everyone loves reading about the Siberian fox experiment because domesticated silver foxes are so damn cute. There’s something deeply appealing about the idea of a cuddly fox. And the experiment raised some interesting questions about domestication. Could domestication really happen in just eight generations? (Apparently.) Domestication must just affect the brain and not the rest of the body, right? (Apparently not – domesticated foxes can have characteristic coat color changes, floppy ears, and curly tails, similar to morphologic differences between dogs and wolves.) But a research population of domesticated foxes hasn’t been maintained since the sixties just because they are cute. We’re still learning things from them. Like what? Get ready for some well-aged papers; a lot of this work was done back in the eighties.

Hormone and neurotransmitter soup

We use the hormone cortisol as a marker of stress: if you have more cortisol in your blood, you’re probably more stressed. It turns out, perhaps not surprisingly, that domesticated foxes have lower basal levels of cortisol than their unselected counterparts (Oskina, 1992). Their cortisol levels also don’t go up as high during a stressful experience as do the cortisol levels of unselected foxes (Harri, 2003). Personally, I think cortisol is going to play a key role in the mechanism of why domesticated animals are less flighty than wild ones. Cortisol levels influence the production of adrenaline: if you have more cortisol in your system, you are liable to make more adrenaline (Kvetnansky, 2009). If you have more adrenaline in your system, you are going to react more strongly to scary stimuli – in other words, your flight distance is going to increase. (Quick review – domesticated foxes were bred by selection for decreased flight distance from humans.) My friends and I noticed during our highly stressful first year of veterinary school, when our cortisol levels were certainly high, that were were inexplicably jumpy. One friend reported that she was so startled by the noise of a dropped glass that she actually screamed.

As for the ever-popular serotonin, the “happy hormone,” domesticated foxes have more of it in their midbrains and hypothalamuses (Popova, 1991). Yes, the same hypothalamus that is the beginning of the hypothalamic-pituitary-adrenal axis, which ends in the release of cortisol. Oh, and which is inhibited by having more cortisol already in the system, in a negative feedback loop.

There is nothing cuter than a baby domesticated fox

Wolf cubs have a much shorter socialization window than dog puppies, and this might be part of why it is so difficult to socialize a wolf cub to humans. It turns out that unselected fox kits have a shorter socialization window than domesticated fox kits, too. Prime socialization time in both lines seems to start around 30-35 days, when the kits can see and hear and are mobile enough to explore their surroundings. Like most very young animals, fox kits of this age aren’t as fearful as their adult counterparts; they have a chance to learn what is dangerous and what is not in their particular environment. A longer socialization window gives you more chances to learn that a variety of beings are not dangerous to you, but in the wild it also gives you a greater chance of getting eaten by something that is dangerous to you when you wander up to say hello to it.

Domesticated fox kits start showing fear of new objects after age 60-65 days. Unselected kits, on the other hand, start fearing novel things at day 40-45 (Belyaev, 1985). We don’t know what exactly causes this difference in a preprogrammed socialization window, but it’s very helpful to have these populations as we look for the cause.

An even lower level of programming

In recent years, researchers have had new tools to use in exploring the mechanisms of domestication in foxes, especially since the canine genome was sequenced. Comparing gene expression in the wolf and the dog is problematic, because they necessarily live in such different environments. Comparing gene expression in two populations of foxes raised in identical conditions is potentially much more fruitful. This research is in the early days. But as we learn more about the canine genome I think we’ll start finding some really interesting differences between the lines of domesticated and unselected foxes. My personal belief is that we’ll find subtle differences – maybe, rather than differences in actual genes, we’ll see changes in promoter sequences, which cause significant genes to be up or down regulated.

We’ve learned a lot from the Russian domesticated foxes so far, but we have a long way yet to go. We still have no real idea exactly what is at the root of the difference between a domesticated and undomesticated animal. Does the change in development affect cortisol and serotonin levels, or vice versa? Does just a single genetic modification cause all the physiologic changes we see? Or are we looking for a set of modifications? Hopefully the new genomic tools we’re developing will allow us to get to the bottom of the mystery.

References

OSKINA, I., & TINNIKOV, A. (1992). Interaction between cortisol and cortisol-binding protein in silver foxes (Vulpes fulvus) Comparative Biochemistry and Physiology Part A: Physiology, 101 (4), 665-668 DOI: 10.1016/0300-9629(92)90341-M

Harri M., Mononen J., Ahola L., Plyusnina I., Rekila T. Behavioural and physiological differences between silver foxes selected and not selected for domestic behaviour. Animal Welfare. 2003:305-314.

Kvetnansky, R., Sabban, E., & Palkovits, M. (2009). Catecholaminergic Systems in Stress: Structural and Molecular Genetic Approaches Physiological Reviews, 89 (2), 535-606 DOI: 10.1152/physrev.00042.2006

POPOVA, N., VOITENKO, N., KULIKOV, A., & AVGUSTINOVICH, D. (1991). Evidence for the involvement of central serotonin in mechanism of domestication of silver foxes Pharmacology Biochemistry and Behavior, 40 (4), 751-756 DOI: 10.1016/0091-3057(91)90080-L

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