Briddle Creek Working Terriers
Where did those black puppies come from?

This is the case of Rushill Gambler, a Jack Russell Terrier imported from England. He is registered as tan/white, but his color is something of a dull red (Figs A and B). The color was more yellow when he was a puppy (Figs. C and D). His sire is a normal tan/white, and his dam is black/white. He has a littermate who was imported with him, and that dog is a normal tan/white (Figs. E and F). But Gambler has been bred to eight bitches -- one white, one tan/white, one black/white and the rest tricolor -- and consistently throws black/white puppies (Figs. G and H). Gambler's owner (Debbie Johnson) does not have any black/white dogs in her kennel, and the breedings -- all but one to outside bitches -- have been carefully monitored.

   Total puppies: 37
   Tricolor: 23
   Black/white: 13
   Tan/white: 1
For readers of this article who aren't familiar with Jack Russell color patterns, you must understand that this goes against all conventional wisdom. It is widely understood that at least one parent must be phenotypically (visibly) black/white in order for any of the puppies to have that coloration. One exception is when the white patches on a tricolor terrier cover the tan-point areas. This is not the case in Gambler's puppies, a few of which are heavily marked. Another exception is when a young terrier appears to be black until adulthood and the once-black patches take on a reddish hue when viewed in sunlight. This also is not the case with these puppies, which have retained a solid, deep black into adulthood.

According to geneticists Clarence Little and Malcom Willis, there are about 9 gene pairs that determine coat color and pattern. They are referred to as A, B, C, D, E, G, M, S and T. The B series determines whether a dog expresses black or liver, the C series affects melanin formation, the D series is dilute, the G series affects graying, the T series affects ticking and the M series is for the merle pattern. These don't really matter in this case, because we know Gambler isn't liver, merle, dilute, gray, ticked or albino.

The S series is what gives Jack Russells their white coloring. There are two alleles that cause white spotting and they carry plus and minus modifiers that determine how much white there is. The two alleles are sp and sw, so just for argument's sake, we'll say Gambler is sp sw for white spotting.

What we're interested in are the A series and the E series.

The A (or agouti) series, has five alleles. This is where you get your self coloring that allows for black and the alleles for tan or tan-point (black and tan). Listed below are the five alleles in order of dominance:
A: dominant black
ay: dominant yellow (also called golden sable. It is tan in JRTs)
ag: wolf grey
as: bicolor with saddle markings (like a German Shepherd)
at: bicolor with tan-points (like a Manchester Terrier or Doberman)

In order to produce black puppies, Gambler must have at least one A allele. He also consistently produces tricolors, so he must also have the at gene. So Gambler, being Aat, should appear as a black/white dog.

The E series regulates the extension of black pigment and has four alleles. They are listed in order of dominance.
Em: super extension with black mask on face
E: extension without black mask. This allows for expression of black pigment, and I believe that nearly all Jack Russells are homozygous for E.
ebr: brindle
e: restriction. This keeps black pigment from expressing itself except in the nose and dark eyes, even if the dog carries the genes for that pigment. According to Willis and Little, recessive red dogs can exhibit a wide range of coloration -- from yellow to deep red. These dogs, despite the dark pigment in the nose, have the tendency to get a "snow" nose during winter months where the nose takes on a pinkish cast. I believe that Gambler is ee.

This is what Willis ("Genetics of the Dog", Page 68) has to say about how the recessive e works with the A series:

   "The effect of e is concealed by Em, E or ebr because all three are dominant to it. However, in a homozygous state ee acts upon the agouti series in various ways. With as or at alleles in any kind of combination the ee structure will cause all black pigment to disappear except in the nose and the dog will be tan marked but with a different shade of tan in those areas that would normally be tan marked in black and tans."

Coupled with AA or Aay, Aas or Aat the ee factor will also cause black pigment to disappear, but in this case it will lead to a clear, uniform red-yellow pigment throughout the animal. Thus we can have two different kinds of red or yellow dog. One kind stems from A-ee while the other kind is ayayEE. Fawn Boxers are examples of ayayEE reds while yellow Labradors are AAee animals."

Little says on Page 60 in "The Inheritance of Coat Color in Dogs:

   "When an animal is ayay [sable-tan], the E gene has little dark pigment on which to work. Sable dogs probably represent a conflict between E, which attempts to form or extend dark pigment in the coat, and ay, which attempts to restrict or inhibit its formation. It is possible, therefore, to have ayayEE animals that are all shades of sable including clear tan and that, when crossed with AAee reds or yellows, recreate a solid, dark colored dog, AayEe."

I believe that Gambler's reddish color, coupled with his ability to produce black/white puppies, indicate that he carries the black A gene and the recessive ee alleles that restrict its pigment. In other words, Gambler would be a black/white dog if he did not have the genes that restrict black pigment. Bred to normal EE bitches, some of his offspring get his A gene and are Ee, and therefore are black/white.

Take a look at the Punnett square in Fig. I showing Gambler's ee paired with a bitch's EE. One hundred percent of the resulting puppies are Ee, meaning they possess full pigment and carry the recessive gene that restricts pigment. Bred to similar heterozygous animals, they will produce ee dogs like Gambler.

Now let's look at the Punnett square in Fig J showing Gambler's color genotype, Aat, paired with a tricolor bitch, atat. The statistical results show that 50% of the litter will be black/white and 50% will be tricolor. All of those puppies are Ee and show full pigment, so their genotypes are this:
atatEe Tricolor, carrying one recessive e gene
AatEe Black/white, carrying tan-point (tricolor) and one recessive e gene

One of Gambler's daughters has reportedly produced puppies with very light yellow markings. She was bred to another English-bred terrier, but not linebred to her sire or any of his close relatives.

The only potential discrepancy I see in this case is that the percentage of tricolor puppies to black/whites is higher than it should be. Statistically, as an Aatee, roughly half of the puppies Gambler produces should be black/white. However, he has produced 62% tricolors, 35% black/white and 3% tan/white.

Is this an isolated case, a result of a mutation?
I'm not sure, but I doubt it. I have been in touch with another individual who produced black/white puppies under similar circumstances. The bitch has what her owner describes as "pale tan" spots on her ears, but her markings were so slight it was difficult to assess the color in the photographs I saw. The bitch's sire was black/white and her dam was either tricolor or tan/white. She was bred to a tan/white terrier, but all the puppies were black/white. The only explanation seemed to be that a black/white 8-month-old puppy had gotten to the bitch. The bitch has only been bred the one time, so there is no basis for comparison. She has a different pedigree from Gambler.

Where would the e gene come from?
The Jack Russell Terrier largely is a recreated breed and most dogs owe their ancestry to other breeds such as Beagles, Fox Terriers, Border Terriers and working Lakeland Terriers, among others. The e gene is thought to cause lemon in Beagles and red in Lakelands. Incidentally, there is a red Lakeland bitch, Floss, who appears twice in the fourth generation on the sire's side of Gambler's pedigree.

I certainly don't think that Gambler should be penalized for his color because he does fall under the broad spectrum "tan," although it would be more accurate to call him "red." He has the black nose and dark eyes required by our breed standard.

Bibliography "Genetics of the Dog", by Malcom B. Willis. Howell Book House, New York. 1989.
"The Inheritance of Coat Color in Dogs", by Clarence C. Little. Howell Book House, New York. 1957.


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Figs. A, B
Gambler: Recessive red

Figs. C, D
Gambler as a pup

Figs. E, F

Figs. G, H
Gambler puppies

Fig. I
Punnett square 1

Fig. J
Punnett square 2

Litter #1 Whelped 10-24-99
Dam: Tricolor bitch
1 b/w male
3 tri females
Litter #2 Whelped 1-21-00
Dam: Tricolor bitch
1 b/w female
2 tri females

Litter #3 Whelped 3-23-00
Dam: Tricolor bitch
1 b/w female
2 tri males

Litter #4 Whelped 06-30-00
Dam: Tan/white bitch
2 b/w females
2 tri females
1 tri male
1 t/w male

Litter #5 Whelped 7-19-00
Dam: Tricolor bitch
2 b/w males
2 b/w females

Litter #6 Whelped 7-20-00
Dam: Tan/white bitch
2 b/w females
2 tri females
2 tri male

Litter #7 11-14-00
Dam: White bitch
1 b/w female
2 tri females
1 tri male
Litter #8 Whelped 12-7-00
Dam: black/white bitch
1 b/w male
3 tri females
3 tri males

How do you explain black/white Jack Russell puppies being produced by non-black/white parents? Most people assume that the wrong sire got to the bitch. But what about a dog that is completely lacking in black pigment, except a black nose and dark eyes, which throws at least one black/white puppy in every litter he produces?