Color Inheritance in the Boerboel

PART ONE – Existing Colors in the Breed

It was my pleasure to deliver a series of illustrated lectures in the Republic of South Africa at the invitation of a coalition of the South African Boerboel clubs in January 2011. One seminar was on the subject of hip dysplasia and other orthopedic disorders, and the other was on gait and structure. The first set was in the Johannesburg-Pretoria area, and the following weekend it was near Durban on the Indian Ocean coast. Both were attended by enthusiastic groups of novices and experienced breeders representing the three or four Boerboel breed clubs in the country as well as fanciers from Belgium and the United Kingdom. After the slide presentations, we discussed general questions including inheritance of other traits besides orthopedic ones. It is the aim of this article to attempt to clear up some confusion that I recognized as existing in the fancy, about coat and pigment color inheritance.

With such a wide range of experience and scientific knowledge in the field, it was easy to see how different people have different ideas when the subject of allowable colors is brought up. Please realize that I am not trying to steer the Boerboel into any personal-preference path. I have no vested interest in the outcome of your decisions. Instead, I offer an outsider’s view, but also one that is based on over 70 years of experience with dogs, and almost as many years of serious study in the field.

It’s always important to define terms. Not so much as to change any one person’s lexicon, as to establish a common language so that all parties know what is meant when words are used. For example, what is your definition of “color”? How about “pigment”? As long as one’s audience understands the context, the words used will also be understood. Also, it helps if you narrow your field by adding a modifier word, so that you get agreement on what is being referred to when you use terms such as “coat color” or “nose pigment.” Additional confusion can occur when we use the same word for both types of pigmented areas of the body – that is, both the hair and non-hair areas. By the way, I trust you understand my American spelling of some words such as color instead of the British “colour.”

Most of the time, I prefer to use that word (color) for the coat, and “pigment” to refer to such outer-integument (skin) areas as the nose bulb, eye rims, lips, footpads, anus, and sometimes nails. But you can use the words interchangeably and still be understood.

Before going to South Africa, I did not realize that there were black specimens in the breed. Whether this was in the breed from the beginning, or whether it is widespread or principally one breeder’s production is almost immaterial, as it appears it is in the breed now, and it might be detrimental to the clubs and to the breed if a purge were initiated. The same can be said for some pigment variations that we call “dilutes.” Most Boerboels I have seen have black-pigmented noses and other integument areas, although the great majority have a base coat color of tan (you can call it fawn or red, or use a few other terms) that ranges from a light coffee to a deep dark hue. White markings may be present, but for now, discount these when speaking of color. They are caused by different genes than those we are talking about for base coat color.
Animals have a pair of genes in every cell that code for a certain characteristic, in this case, color. It is convenient to give an alphabetical nomenclature to them in the places (loci, plural of locus) on the chromosome where those genes are located. Geneticists have not always agreed on what letters to use, but I like the abbreviations or symbols used by Dr. Clarence Little, for the most part, and you can use your own words: “A” might refer to “Agouti” or “All-over” pattern. “B” for Black if capitalized (or subcase “b” for the shade of brown generally called liver). “C/c” for concentration of color. “D/d” for Dark and dilute (blue). E/e for the extension alleles that govern the distribution, if any, of black pigment granules. And there are more.

We find it convenient and helpful to use a diagram such as shown below, to show relative dominance of alleles. Remember that alleles are different variations of the basic genes that are at specific positions on the chromosome, and determine colors sown in the integument. Normally, capital letters are used to represent the most dominant of each series, and the subcase letters under them refer to progressively less-dominant (recessive) forms or alleles of each type of gene. Different geneticists may use slightly different abbreviations, but the relative positions/dominance should be the same in all texts. In almost all literature, you will see a capital letter E used for full expression or extension of black in the coat. The most-recessive allele in this series is e , restricting (refusing) any expression of black. The subcase letter means it is recessive to some other allele. In between, there is e^br for brindle. Some breeds have only one or two of these choices.

Consider the horizontal order of letters in the illustration below to represent different locations along a straightened-out chromosome, and the vertical arrangement to represent decreasing dominance. Choose only one in each vertical column, for each genome (in a sex cell or gamete). The order of dominance is according to Dr. Clarence Little, based on information from similar breeds.

Figure 1: Probable Gene Map for the Boerboel Breed and Many Others

As	B	C	D	E	S
ay	b	cch?	d	ebr	si *
		?		e	sp **

The above diagram indicates that at the A locus, there might be either the most dominant “solid” pattern allele, A^s , that allows for dominant black to be expressed, or else the ay recessive allele that codes for yellow-red and does not allow any black regardless of what is called for on other loci. At the E locus, we have the choice of full Expression of black, denial of black expression, or partial expression in the brindle pattern. A black Boerboel would have to possess at least one A^s , and at least one E allele. The red-fawn dogs have a^y at the A locus, but we don’t know what E-locus alleles it has until we do enough test breedings, especially to black dogs.

The C locus affects the depth of yellow-red coat pigment, not its presence or absence (though two ch “chinchilla” alleles might produce near-white dogs in some breeds). Neither B nor D (the density-dilution loci) would have any effect on spotting. The white-spotting alleles that give us piebald Boerboels do not seem to have any noticeable effect on the red or black coat, either.

So, we have two or three possible explanations for the “yellow” (fawn, tan, red) dog in the Boerboel breed: 1. It could be A^see , the combined presence of the dominant black allele at the A locus but with two copies of the recessive “non-extension” allele e at the E locus: the A^s would try to demand a solid black, but the e on the other locus does not allow that color to be extended to the haircoat. 2. Another possible cause for the very common tan color is the combination a^yE , wherein the A locus calls for yellow instead of black, even though the E calls for “extension” (of black, normally). 3. It could be a^ye , which would normally be indistinguishable from #2. You need both A^s and E to make a black dog. Lacking either capital-letter allele would give us the red dog. The problem is, that until enough breedings are done with accurate pedigrees in regard to colors, we may not know which of those we have. It is possible that all scenarios exist in the Boerboel to further confuse the breeder. Incidentally, in some breeds (Brittanys, Vizslas, and more), there are no specimens with black coat hairs or black integument (nose bulb, eye rims, lips, etc.).

In breeds that have black hair on part or all of their bodies, the integument will be black. When thinking about the genetics of color, don’t concern yourself for now with such things as “snow nose” or other ancillary, temporary, and minor variations. A black-coated dog will have black integument. Most Boerboels with no black in the haircoat will also have black color on their noses and those other non-hair parts listed above. If a dog has a double dose of the d allele in place of the dominant D allele at the D locus, such a dog will be blue (in the integument). If one of each, we say that he is genetically and black in phenotype, but carries the dilute (blue) recessive. If he has both alleles at the D locus expressed as d , he will be dark slate-blue in both the coat and integument places that DD or Dd dogs would be black. In many other breeds, there are black-nose dogs but no dark hair except in the pattern known as brindle. In those non-black-haired dogs, blue could only be seen in the integument.

Since the dilute form of D is recessive, blue-nose dd dogs will continue to pop up in breeds where it has previously existed, despite moves to make it a disqualification. Since it has been in the Boerboel gene pool probably for as long as the breed has been developing, I recommend that it not be discriminated against. Certainly not made a disqualification (DQ)! There is no health problem associated with the blue recessive, and since there will not be any dogs with blue replacing the red-fawn coat color when two such are mated, I advise that a merging international South African Boerboel organization leave blue in the Standard.

The same advice can be given in regard to the “liver gene” that in bb (we call this double dose “homozygous”) substitutes this chocolate-brown color in those hair and integument areas more customarily seen to be black. In the case of such breeds as the Vizsla, Redbone Coonhound, Dogue de Bordeaux, Brittany, and other bb breeds, there are no black-pigmented individuals in regard to either hair or integument. For the sake of genetic diversity in a breed that cannot afford to throw out structurally and temperamentally good dogs, I recommend that the club or clubs not disqualify (or perhaps even fault at all) blue and liver coats or pigment.

PART TWO – Simplifying the Picture (Maybe!)

In Part One, we looked at the “recognized” and existing colors in the Boerboel. Many fanciers of other breeds can easily substitute their breed’s name: Boxer, Great Dane, American Staffordshire Terrier or American Pit Bull Terrier, Greyhound, Basenji, etcetera, and apply these principles. Now, let’s get into a bit more detail and dispel some misunderstandings. First, we start with some simple generalizations and agree on terms used.

When discussing the black dog, don’t get hung up over the fact that some of these dogs are not a pure jet black. It is common to see a reddish bronze tinge to a portion of the coat in some Boerboels, Newfoundlands, and others, as if slightly sunburned. Or a faint dusty impression as if a tiny portion of the hair shaft is rusty. In good lighting, this can be more easily seen when comparing that area or dog standing next to one with a more pure black topcoat. A Boerboel breeder south of Johannesburg told me, “People call me from time to time to report that a black puppy was born in a tan litter from tan parents. I have never seen any of them and the reason might well be that it was always a roaming father!” He also said, “Some of the black dogs have a tendency to fade in parts of the coat.”

Fading of black coats (a tinge of rust or brown in some part of the hairs) can be caused by several things: a recessive gene for liver-dilute pigment, or modifier genes located on different places or chromosomes, for example. Or, minor differences in same-color dogs can be caused by environmental influences, such as exposure to much ultraviolet light (sun) or diet (often, an exceedingly high level of protein in commercial dog food). This is often referred to as “bronzing.” Although the visual effect can be the same, it is easy to confuse this with the subtle hint of bronze (liver) that shows through in coats of some black dogs that carry an incompletely-masked recessive allele (one of the gene pair) for “a dilute” such as liver-chocolate. A black dog with a tinge of color is still genetically a black dog.

There is a saying that for every rule, there is an exception. It is highly unlikely, though not absolutely impossible, for a black dog to spontaneously appear in breeds or lines that have never before (to anyone’s knowledge) produced a black. Dr. Clarence Little reported it in a carefully bred number of litters of Irish Setters — one pup out of 1200 in that controlled breeding program. He considered it an extremely rare mutation, changing the dog’s genes from “e” (the gene denying black) to “E” (the gene requiring black). You should, for practical purposes, consider that non–blacks will not produce blacks.

Now, let’s get back to the subject of what colors are in dogs’ coats and non-hair integument. While birds, butterflies, and flowers can have a great range of true colors, you can consider dogs as having only two colors: black and yellow. Before you start arguing, try to see that black and liver (chocolate) are simply modifications of black pigment granule arrangements in the cells. And that the granules producing yellow (tan in various shades from almost white to dark rust-red) occur in different hair shafts or else in different portions or bands on any shaft than where those causing black are deposited. Thus a yellow Lab or red-tan Boerboel will have hair pigment granules reflecting wavelengths of light in the red-yellow range of the spectrum. A black Lab or Boerboel will have a different type of pigment granule in those hair shafts. If beginners want to get confused, they can think also of breeds like the German Shepherd Dog that usually have two or three different-color bands in the same hair shaft.

Before going further, give yourself a vocabulary lesson. Black is black, but the other colors in dogs’ hair have many names, varying by breed and the writer’s or speaker’s experience. However, all of these (other than the dilutes of black) refer to the same area of the color spectrum: yellow, gelbe, tan, fawn, orange, red, rust, mahogany, etc. Even most dogs that appear white are really extremely faded yellow dogs: light-cream Labrador or Golden Retrievers, some white German Shepherds, and others. On the other hand, it may be that Samoyeds, Pyrenean Mountain Dogs, Sealyhams, and some other breeds are white because of extreme white-spotting genes such as we see in the Bull Terrier. The fact that there are two routes to a white phenotype is mentioned, but we won’t go into detail here because this article has been prepared primarily for the Boerboel and breeds with similar color patterns. Get used to the various descriptions being used to refer to the same genetic and histological color range. The word “yellow” is used by geneticists far more than those other descriptions.

When we refer to that yellow or red-fawn coat color in the Boerboel and many other similarly-colored breeds, we could include the white-marked dogs that have portions of their colored coat replaced with white markings (patches where pigment is lacking). This type of white spotting varies from dogs with a few hairs on the chest, to those with white feet and a chest blaze, to dogs patterned like Frisian or Holstein cattle, to the apparently all-white Bull Terrier with a tiny spot on an ear or eyebrow, to some dogs that appear to have no pigment in their coats at all. It is very likely that the genetic cause of such dogs is different than what causes absence of color in other breeds. The partial spotting that we see in some Boerboels, hounds, and many others is known by various names, depending on amount and convention: Irish spotting, piebald, and “extreme” all-white are commonly-used terms. It almost certainly has a different cause than we see in white German Shepherds and some other breeds.

The subject of white coat color is confusing to perhaps a majority, even experienced dog-show exhibitors. Mostly this is because they tend to think of white as a color. In terms of pigment, white should be thought of as an absence of color. To a physicist, white light contains all the colors of the visible spectrum, but to most of us, “colorless” and “white” are synonymous. What we see in a red-yellow dog is those wavelengths being reflected while other color wavelengths are absorbed. A black dog in the sun will be hotter than a white dog because less light and heat are reflected by its coat and more heat is absorbed.

Back to black: When I said that black is black, It was to emphasize that it is different from yellow-tan in regard to where it appears on the over-all coat or on hair shafts. Dogs with black saddles, such as Shepherds, Airedales, many hounds and more, have what we refer to as patterns. Whether you want to think of such a dog as being a black with tan underparts or markings, or if you call it a tan dog with black saddle markings such as saddle or mask.
While the color black in the Boerboel, Labrador, Great Dane, or some other breed is caused by a gene (more accurately, a gene pair) on one locus of the chromosome, such a gene can have a variation (allele) that codes for a minor difference in how the pigment granules are arranged in the hair shaft or the integument cells. If they are directed (by genes) to be packed closer together in one way, the light will be absorbed and reflected in such a way that we will c all it black. If the arrangement is different in a certain way, the dilution effect will give a slate-grey color variously called charcoal, blue, or perhaps something else, depending on what word the old-timers in your breed decided to use. I and most geneticists prefer the word “blue.”

PART THREE – Liver and Blue Color Variations

Another allele, on a different chromosome locus, can cause the arrangement or packed density of pigment granules to give a brownish color in areas that are commonly black in many breeds: nose, dorsal haircoat, etc. The locus is given the designation B (if we refer to a more recessive allele we use the subcase b ) and you can remember that by associating it with the word Brown, if that helps your memory. Depending on custom in your breed circles, this color may be called liver, brown, seal-brown, or chocolate. When I am with Labrador Retriever fanciers, I usually use their favorite word, chocolate. When with German Shepherd folks, I use the word liver. It is the same allele and expression, regardless. In some breeds wherein all the individuals have the same b allele (the dominant B has been lost) the color is understood but seldom mentioned: Vizsla, Brittany, Dogue de Bordeaux, etc.

The gene (allele) that codes for liver-chocolate expression of the otherwise black pigment is on a different part of the chromosome than is the gene for black/blue. You will remember that we refer to the place where the allele exists that causes black or blue as the D locus: Dark or d ilute. Similarly, when we have alleles that cause liver to substitute for black, we are speaking of the B locus, with B for Black and b for the brown (liver) expression.

These letter designations are simply for the sake of convenience. In any case, it is important to remember that these two (D and B) are on two different locations on the chromosome. They act almost completely independently of each other. Additionally, we must remember that in either location, only one allele of the basic gene can exist at any one time on one chromosome location. Thus, some dogs can have dilute alleles on both the D locus and the B locus, in which case the otherwise black color will show up as a silvery-grey. For example, if a dog has both bb and dd , you would see the silver or pale shade that characterizes the double-dilute Weimaraner and “Isabella” Doberman Pinscher. Breeders of some other species sometimes use the word “lilac”, but I recommend that the Boerboel and other clubs use the term “double dilute” instead of making up another breed-specific word such as has plagued Dobe people. If there are none of these animals, as of the time I write this, they will appear in your breed soon enough. Signs of the presence of both dilutes in one dog that you can expect to see, if you look carefully, include the nose and the rest of the otherwise black areas being slightly lighter or more dusty-looking than you might see in a simply blue dog. Again, it is difficult to see in poor light, so stand the suspected dog next to a blue that does not have both dilutes in double dose.

PART FOUR –Brindles, and More on the E locus

Since black coats represent a rather recent consideration in the Boerboel world outside of South Africa, let’s get back to the topic of the more usually-seen “yellow” dog. Such a dog will carry the genes for arranging pigment granules in the nose and other integument to show black, liver, or blue, but nothing at the E locus that allows anything other than tan hairs (or tan with brindle striping).

The E locus (let’s use E or e to stand for Expression) tells the body whether or not to create and deposit pigment granules that show up as black or dark (including liver and blue) in the coat. The dogs that lack the specific dominant E allele for those dark coats will have hair limited to the various shades of red/tan/fawn (“yellow”). We give them the sub-case designation “ e .” This latter expression gene is what causes most Boerboels to be basically tan dogs. That is, while a dominant E allele is present in black dogs, it is absent in the majority of individuals in the breed.

Making it more complicated, in order to have E express itself as a black coat, it is necessary to also have the A^s allele for self- or solid-black at the A locus. Until many fanciers in the Boerboel world “discovered” the black dog, they assumed that a^y (or A^y ) was the most dominant and perhaps the only allele at that locus in the breed. It appears that for the larger population of the breed (i.e., in most kennels and households), the A^s allele is not (yet) present.

In most breeds, the E allele is the most dominant, but in some breeds (or some populations/bloodlines within a breed) it is absent. There might be some question as to which is next in order of dominance, the e^br allele for brindle (the br should be written as a superscript), or the e allele (no superscript) for non-expression of dark hair pigment. Brindle is seen in Boerboels, Danes, Boxers, Greyhounds, and numerous others. This allele produces that tiger-stripe effect that ranges from barely noticeable (and easily missed, especially in dogs with much white-spotting replacing colored areas) to so concentrated that the dog appears to be a solid black (Scottish Terriers). The striping effect is caused by part of some hair shafts being black, but in a unique pattern. The more or the less of the parts of the shafts being dark make the difference in over-all dark appearance of the brindle dog. If a brindle dog is seen, you can be sure that both parents carry the brindle factor and have contributed it to that dog. German Shepherds, Retrievers, Pointers, and numerous others do not have brindle individuals yet can have black hair on parts of their bodies, in a different pattern. In any case, brindle is recessive to black self-color and to saddle patterns (as in GSD, Airedale, Rottweiler), and possibly to the yellow e -allele dog as well.

In other breeds, brindle e^br reliably seems to be recessive (hypostatic) to E . I got the impression from some people in SA that in the Boerboel, it was thought to be dominant, and it appears that this is a common misconception, or incomplete, at least. The same idea is common in Boxer circles, and genetics in that breed is similar. Brindling may be hypostatic (recessive) to E , but probably not to e. It seems that, as in other breeds, the br allele lies in between those other two alleles in terms of dominant/recessive “power.” If you repeatedly breed a certain pair of brindles, and none of their offspring are red-only, then at least one—maybe both—of the partners is almost certainly homozygous for the brindle factor ( e^bre^br ).

In order to say that dogs are capable of producing a solid-color coat, they either must have at least one copy of A^s (they are black dogs), or they have a pair of a^y alleles at that locus (solid, but red-yellow), or they do have an As but not an E to express it (they only possess ee and thus are also solid reds). To produce brindle offspring, dogs must have, in their pair of E-locus alleles, at least one copy of e^br . Vincent Marvell and Sonia Morgan agree, saying, “You need a brindle parent to produce a brindle pup. In our experience, two non brindles, even those with brindle parents, have never given brindle puppies.” But neither of them has bred black dogs. It is probable that a self-color black with a suppressed brindle allele (genotype A^sa^yEe^br or A^sA^sEe^br or A^sA^se^bre^br ) would produce brindle pups if mated with an a^ya^yEe^br (a fawn that also carries the e^br allele as a hidden recessive) or with an a^ya^ye^bre (an obvious brindle). Some of the pups could be homozygous for brindle: a^ya^ye^bre^br , and some heterozygous: a^ya^yEe^br . To further complicate the matter, it seems that in some breeds, some (but not all) of those heterozygous dogs will show brindle phenotype.

Marvell and Morgan add, “There has been one very dark brindle Boerboel called Vanson Yster who was called a ‘dominant brindle’ because all the pups in all litters he sired were brindle, even when mated with non-brindle bitches.” However, I think it likely that those red bitches carried the br as a recessive. Furthermore, if Yster had been used often enough on non-brindle bitches, he might have produced pups with their dam’s coloration sooner or later. It may have been just the luck of the draw, the roll of the genetic dice, that he had not (yet) had red-fawn pups. The term “dominant brindle” is unfortunate, as it may lead some to think that brindle is epistatic or dominant over E , the gene for extension of dark pigment over the whole surface.

Miscellaneous Comments

Although I initially promised to keep this as simple as possible, genetics is more involved than can be presented to the average audience or readership, and there are sure to be a number of readers who still have questions. The website addresses at the bottom of this article may be helpful for further study. But in conclusion, I’ll try to lightly touch on a couple of minor things you may have been wondering about.

Claws (the more common word among non-veterinarians is “nails”) are extensions and modifications of hair. Both stem from the same embryonic path that leads from fertilization to birt