The star coat pattern in foxes: what does it have to do with tameness?

Despite my previous voracious reading about tame foxes, as I settle in to my new lab I’m realizing how much I don’t know about them. For example, one of the most interesting things about the tame foxes is that although they were selected just for behavior (not running away from a human approach), they have physical changes as well, and those changes mimic physical changes between wolves and dogs: the appearance of white patches of coat color, floppy ears, and curly tails. I have learned that this is not an example of white patches related to tameness:

Platinum fox

That is a platinum fox, a color morph unrelated to the white coat markings that seemed to appear with tameness. The white coat markings come from the star gene. So what do we know about the star gene? What do those markings look like?

I started my hunt for information about the star gene in my own reference manager, since I knew I had read about it before. The only paper I had saved about it was from 1981 (!) but it was written by the mastermind of the farm fox project, Dmitri Belyaev, so it seemed like a good enough place to start.

Belyaev D.K. (1981). Inherited activation-inactivation of the star gene in foxes: Its bearing on the problem of domestication., Journal of Heredity, 74 (4) 267-274. URL: http://jhered.oxfordjournals.org/content/72/4/267.short

So back in 1981, when rock music was just starting to get really good, Belyaev was pondering the trickiness of the star gene. At that point, the tame fox project was only 20 years old. In 1969, the first white-spotted fox was born on the tame fox farm, with spots on his head and paws. Other foxes followed. The images from the paper show them looking like this (apologies for the poor image quality — it’s all I have to work with):

Fox kits heterozygous for star allele

This star pattern was not completely new. It had appeared on other fox farms, in foxes that were not selected for tameness. However, it was appearing much more often in foxes on this farm that were selected for tameness. In fact, the three families of foxes that were the most friendly to humans were showing this color pattern the most often. Unselected (not tame) foxes showed this star pattern 1.1% of the time, on multiple farms. (This includes foxes on the experimental farm which were from lines that were not selected for tameness.) Foxes in tame lines showed the pattern 3.7% of the time, or more than three times as often.

By the way, the fox kits shown above have only one copy of the star allele. Animals with both copies of this allele look much more like border collies:

But you can see how the non-white parts of their coats are a dark silver, unlike the platinum fox pictured at the top of this post.

Anyways, the question was: why were the tame foxes showing this pattern more often than conventional foxes? The pattern is particularly intriguing because it looks so much like the patterns we see in coats in domestic dogs, as well as in domestic horses and other domesticated animals. Was it possible that whatever mechanism was making these foxes more friendly to humans was also affecting their coat? The other explanation is just as likely but a lot less interesting: that when foxes were selected for tameness, the ones that were chosen just happened to have more copies of the star allele in their gene pool than average. Inbreeding would then cause this allele to show up more often.

Belyaev looked at family trees of foxes showing this pattern, trying to figure out if the gene for star pattern was recessive or dominant. The genealogy he found was somewhat perplexing. It didn’t follow the structure you'd expect for either a dominant or a recessive trait. The trait appeared to have variable penetrance, meaning that some animals with the star allele showed the star coat pattern, but some didn’t have star patterns, despite having the allele for it. This, of course, begs the question: if you have a group of animals, all of whom have the star allele, why do only some of them actually have the star coat pattern?

There are some possibilities:

• There may be a hormonal difference in the tame foxes which changes the effect of the star allele. In other words, the hormonal soup of a tame fox (less cortisol, less adrenaline) may affect coat color during development, so that those foxes are more likely to express the star allele if they have it. Conversely, the hormonal soup of a conventional fox (more cortisol, more adrenaline) may somehow suppress expression of the white spotting.
• The star allele has been around for a while, but perhaps it appeared in lower numbers in conventional foxes because it was somehow inactivated. Something about breeding for tameness may have activated the gene so that it was not “turned off” as often in tame foxes.

In 1981, no one knew which of these stories was more likely. This was before epigenetics was a hot topic, for one thing. But the nice part about reading historical papers like this one is that sometimes the answers to their questions exist in more recent literature. Which I am going to go hunt down now.