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:

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.

French Bulldogs removed from the KC's high profile list

According to the French Bulldog Club, Frenchies are to be removed from the KC's high-profile breed list  (see here). This means the breed will no longer be subject to vet checks at KC champ shows.

The move is intended as a reward to a breed club that has, under the health stewardship of Penny Rankine-Parsons, embraced that there are problems in the breed and the need for research/health surveys.

The problem is that there's no evidence that any of the breed club's initiatives have actually improved the health of the breed.

There is certainly little evidence that Frenchie breeders are willing to give up on a conformation that in the past 100 years has tilted this breed from moderate to extreme brachycephalism... the same health-compromising, dim-witted direction that affects so many of the brachycephalic breeds.  

The Frenchie breed standard in fact calls for a "well-defined" muzzle, but in profile the breed now has practically no muzzle - a far cry from some of the dogs of old. 

Left: BOB French Bulldog 2011. Right:French Bulldog 1917

As the English Club's own advice on health spells out: "Being a brachycephalic breed that is fairly short and compact with a screw tail, the 'Frenchie' is prone to the associated problems these conformational characteristics will bring."

Of course. It's immutable. Set in stone. 

Have a look at the dogs being exhibited by current top winning kennel, Glenlee - including the Crufts 2013 winner, Renuar New War Bonnet. You can see their current showteam here; it boasts a veritable smorgasbord of stenotic nares.

The 2004 KC/BSAVA survey found that 53% of French Bulldogs suffer one or more health conditions and that the median age of death is 9 years old (only two thirds of the "lifespan of around 12-14 years on average" claimed by the French Bulldog Club of England).

Additionally, many can't mate naturally, over 80 per cent of the breed is delivered by C-section (ref here) and there is a neonatal puppy mortality rate of around 30 per cent.

Yep, this breed doesn't want to mate, doesn't want to be born and does its level best to die if forced into it.

Have a look at this American breeder's site for some eye-watering honesty about French Bulldogs.

It also states, as if it's bad thing: "Bargain-priced French Bulldog pups are bred for from large, long-backed, small-headed, out-at-the-nose French Bulldogs who can breed naturally because of their longer backs and legs. Puppy mills prefer them like this because the small-headed pups they produce can free-whelp without need of a costly cesarian making them more profit."

And just so we can tell the difference, there's a helpful illustration comparing the dreadful small-head, longer-nosed, free-mating, free-whelping ones and the desirable huge-headed, flat-faced, artificially-inseminated, c-sectioned ones.

Apparently, you're supposed to want the one on the right.

Despite all this dysfunction, only one winning Frenchie in the UK has failed a vet check since the KC introduced them in 2012.  But don't be surprised -  the vet checks are pretty much rubbish,  sufficient to pick up lameness or an obvious eye or skin problem, but useless at picking up anything more fundamental, including exercise intolerance due to underlying brachycephalic obstructed airway syndrome. The vets are not allowed to put a stethoscope on the dogs and the dogs only have to trot up and down a few yards. Winning dogs are also often carried/wheeled from the ring to the vet-check to give them the best chance of a pass.

So, if the vet checks are mostly a PR exercise, does it matter that the breed is now exempt?

Yes it does because removing Frenchies from the high profile breed list sends out a strong message that the breed is OK when it isn't - and at a time when KC registrations of this breed are soaring. And it also sends out a dangerous message to others on the high profile breed list - i.e. looking like you're doing something to tackle health problems is good enough.

Even more infuriating is that this morning the Dog Advisory Council - the independent body set up to monitor and find ways to improve dog health post Pedigree Dogs Exposed - has congratulated the breed club for being relieved of what it calls the "stigma" of being on the high profile breed list, as if somehow the Frenchie didn't deserve such a label.

This makes no sense at all. The Dog Advisory Council has stated clearly that it thinks the vet checks are "flimsy" and should be replaced with something much more robust. Why then should removal from such a meaningless test warrant any congratulations? And why would it see being a high profile breed a "stigma" rather than, say, an opportunity?

The answer? I suspect it's that the Council's David Sargan is working closely with the breed club's health rep, Penny Rankine-Parsons, on a Cambridge Vet School initiative to find a way to measure respiratory function in brachycepahlic breeds. (For more info see here.) It is a commendable project - and the French Bulldog breed club has been much better than the Pug Club in offering support.

All good stuff.

But this doesn't take away the fact that the French Bulldog is a fundamentally unhealthy breed.

I've had an exchange of views about this today on the DACs Facebook page. David Sargan has admonished me for being ungracious in not recognising all the wonderful work the breed club is doing. He also suggests that the most extreme health problems may reside in the swathe of imported puppies from Eastern Europe - something that could be true but for which there is no supporting data.

I have accused Sargan of drinking the breed club Kool-Aid; his perspective shot by the close contact with a handful of people in the breed who are making the right noises (something I've seen so many times). That's not to say that I am dismissive of the measures the breed club is taking to improve breed health. I'm not. It's just that there is no evidence that any of them have been effective as yet (after all, how could they, when most of them are so new?)

And, anyway, the measures don't go far enough.

Frenchie breeders need to give this breed back some muzzle. The club also needs to state emphatically that dogs that have had surgery to correct breathing problems should never be bred from - instead of its current advice that they can be used as long as mated to a more sound dog.

Stenotic nares need to be severely penalised.

The breed standard should also (as does the FCI standard) call for taillessness, or too short a tail, to be a disqualifying fault and an effort made to breed for a longer back. All Frenchies used to have a tail. But in the pursuit of a shorter body/spine, it has been largely lost, leading to several health problems (see here).

1899 French Bulldog -  described as being "first-rate in skull and body properties"
(Picture courtesy:Pietoro's Dog Breed Historical Pictures)
2013 - top-winning Eastonite Hurricane
It's quite a difference, isn't it? And I can't see a single change here that is functionally beneficial to the dog. Earlier dogs had a smaller head, wider nostrils, longer muzzle, longer legs, longer spine and tail. And they whelped naturally because routine C-sections for dogs are an entirely modern phenomenon.

After all, if you were a dog, which would you prefer to be... This one, from 1925?

 Or this one?

Crufts 2011

Fox colors

Tame fox kits
We often talk about the tame foxes as “silver foxes,” but in fact there are multiple color morphs in the tame population, not just silver. All of the foxes you’ll see here are the same species, Vulpes vulpes. The silver color morph was the color used for the first foxes which were selected for the creation of the tame population, but other morphs were brought in later.

Here is the silver morph, the color we are all most familiar with as being the color of a tame fox:

Tame silver foxes

My personal favorite fox color is Georgian white. The picture below is the one on my phone background.

Tame Georgian white fox

The ones that look so much like they have border collie markings, which are that lovely lighter silver color, are counterintuitively not called silver; they’re called platinum:

Tame platinum fox
And, of course, there’s the traditional red color, which somehow always surprises me the most to see on a tame animal:

Tame red fox
A rainbow of foxes!

Open access dog salivary cortisol data

I finally got around to sharing the data from my study of dog salivary cortisol levels on figshare. I have meant to do this for months. Particularly, I wanted to do it so that I could wear the cool “I’m a figsharer!” t-shirt that Mark Hahnel gave me at scio13. How embarrassing would it be to wear that shirt and have someone ask what you shared and have to admit that you still haven't actually shared anything? But I am a figsharer now. So if you want numbers, go check it out.

Oh, and in case you’re interested in the associated paper, that’s here (but, sadly, not open access):

Hekman, Jessica P., Alicia Z. Karas, and Nancy A. Dreschel. “Salivary cortisol concentrations and behavior in a population of healthy dogs hospitalized for elective procedures.” Applied Animal Behaviour Science (2012).

Nice to meet you

Having gotten somewhat settled in my new program, I asked my boss how she might feel about my blogging under my real name. She allowed as how that would be just fine. Hi, I'm Jessica. It's nice to meet you.

Which brings me to the really exciting part, which is that I also get to tell you guys that I am privileged to be training in a genetics lab which studies Belyaev's tame foxes! No, really. Where better to be for someone obsessed with the mechanisms behind domestication? We don't have a colony of the foxes here, sadly, but my boss goes to Siberia a few times a year and brings back genetic samples as well as astoundingly cute videos. The lab itself is plastered with photos of foxes playing with things. And the science, obviously, is extremely cool.

I am very lucky to get to work in a lab which works directly with canids. Until very recently, that was nearly impossible to do; in fact, one of the reasons I initially decided to get a DVM instead of a PhD was that I could not find a lab at the time (2007) that would let me work with canids. But dogs are finally getting to be a hot research topic, which has turned out very well for me.

Syringomyelia in pugs

Peppi, the Pug with syringomyelia
Four years ago, Heather from Shropshire called the Kennel Club looking for a Pug puppy. They recommended a breeder in the West Midlands who had puppies on the ground.

Heather called and reserved a fawn pup. A little while later, the breeder called to say the pup had been PTS because of hydrocephalus and offered Heather a black male as an alternative.  Heather agreed and, a little while later, handed over £970 and took the pup home.

When Peppi was 12 months old, he had a fit. Six months later, another one. A check didn't reveal much and Heather was told to wait-see. Some dogs have a fit or two but never go on to develop full-blown epilepsy. And, indeed, that's what happened in Peppi's case.  But by March this year, Heather knew her beloved Pug was in trouble. "He wasn't eating or drinking and I could tell he was in pain."

Peppi was referred to Pearl Vets in Shrewsbury where he had an MRI. The diagnosis? Syringomyelia.

Although the Cavalier King Charles Spaniel is the poster pup for syringomyelia, it has been reported in several small breeds, including Pugs (of all the breeds that cannot afford yet another health problem to add to its litany of issues).

Heather did the right thing - she called the breeder, Michelle Jones of Precious Pugs.  Ms Jones was clearly a little alarmed, revealing that she had kept two others from the litter to breed from. Heather expressed concern about this - after which the conversation got a little frosty. Heather claims it ended with Ms Jones threatened to sue Heather if she started bad-mouthing her breeding.

Heather is very upset about her little dog's suffering. Peppi has been on steroids now since March and although it has helped his condition, he has blown up like a balloon. She called everyone, including the Kennel Club, to complain. And finally she contacted me.

Now note that I am not blaming Ms Jones for the fact that one of the Pugs she has bred has syringomeylia. As I said, it's present in a lot of small breeds and it's perfectly possible that Peppi is the first dog of her breeding that has been diagnosed with SM.

And of course I think anyone that buys a Pug is pretty much nuts. If it isn't syringomyelia, it will be brachycephalic airway syndrome, or hemivertebrae or pigmentary keratitis or luxating patellas or....

But I do object to breeders threatening to sue pet owners for going public with their dogs' health problems - and unfortunately, it happens too often. For the record, it's a meaningless threat. Truth is a very good defence in any defamation/libel case.

So here, for the record, is Peppi's pedigree in the hope that it might join up some dots.

Lots of champions in here - and a lot of inbreeding. The Kennel Club's Mate Select reveals that Peppi (Kenine Ebony King) has a co-efficient of inbreeding of 21% - against the breed average of 6%. Peppi's parents are half-siblings and there are many repeat names throughout this five-generation pedigree.

Click to enlarge