Wednesday, February 26, 2014

The Genetic Factors of Silver Phenotypes


Brian Reeder

First published December 2011 in Exhibition Poultry E-Zine

     What does it take to make a red variety into a silver variety? Most people will simply answer that the sex-linked pheomelanic gene Silver (S) is all it takes, but this is not the case. In fact, getting to a good, clean “white” silver phenotype is much more complicated than simply adding the Silver sex-linked pheomelanic allele to the s-locus. For the last twenty years, I have been working toward understanding the differences in silver and red phenotypes. In that time, I have made hundreds of test matings and raised literally thousands of birds, and with each of those matings, I have gathered data on the segregations of the silver and red phenotypes, in addition to any other data I may have been gathering. By working with such large numbers, I have been able to, first, form a series of hypothesis about the various factors involved in these phenotypes, and second, to test those hypotheses repeatedly and within many different genetic populations, polishing them as more data emerged. Through all that work I have come to a good working understanding of the various heritable factors (genes) involved in these phenotypes.

     In the April 2011 issue of Exhibition Poultry, I wrote an article titled Pigmentation of the Red Jungle Fowl. That article is the precursor to this article, and I would recommend that anyone seriously interested in this article should download the April 2011 issue of this magazine from the website and read over that article as a companion to this one. I will be using my original artwork from that article to illustrate the progression of genes that make the final, fully clean white silver phenotype. I will also be using the MC1R gene, that we call duckwing in the hobby and notate as the e-locus allele e+, as the main base to illustrate this progression from red to silver phenotypes. However, this information does not only apply to the e-allele e+. The exact same heritable factors I will be discussing herein on e+ are used on all the e-alleles to go from the red versions to the clean white silver versions. In time, I will discuss the interactions of these factors on all of the e-alleles, but for the interest of brevity in this article, I will only be using e+ in the examples. The important thing to keep in mind when applying this information to e-alleles other than e+ is that each e-allele distributes the pigments (eumelanin, Sex-linked pheomelanin and Autosomal pheomelanin) in its own unique manner, and more so in the females than the males.

     To begin, let us have a quick reminder of the pigment makeup of the red duckwing, as seen in the red jungle fowl and varieties of domestic fowl similar to it, which I call red duckwing and is commonly referred to in the hobby as black breasted red (image 1). This variety includes eumelanin, the red form of sex-linked pheomelanin (s+), autosomal pheomelanin (Aph), mahogany (Mh) and usually includes dilute (Di). However, the presence or absence of Mh and Di do not change the phenotype from red and these are simply additive genes that create different shades of red/orange.

Image 1 - the typical red duckwing pair which is the color pattern of the red jungle fowl

     In both sexes, Autosomal pheomelanin is the base pigment that lies underneath the other pigments. In the male red duckwing, the body is eumelanin, while the hackle, saddle and main wing triangle are predominantly sex-linked pheomelanin while the shoulder and top of the head show the greatest saturation of Autosomal pheomelanin and also Mahogany (as Mh requires the presence of Aph to express visually – Aph serving as the platform upon which Mh saturates). In the female red duckwing, the breast expresses Autosomal pheomelanin while the back, shoulder, wing, cushion, tail secondaries and sides of the body are a complicated layering/blending of Autosomal pheomelanin, sex-linked pheomelanin and eumelanin. The hackle is mainly sex-linked pheomelanin with a eumelanic stripe in each feather, while Autosomal pheomelanin is predominant at the top of the head and around the outer edge of the hackles. For more on this red phenotype, refer back to my April 2011 Exhibition Poultry article mentioned above.

     So now, if we simply add the sex-linked silver gene to the red duckwing, what does the phenotype become? To begin with, it does not become an exhibition silver duckwing. The female can only have one dose of this z-chromosome, sex-linked gene, while the male can have one or two doses. (We will only be discussing the homozygous silver males (S/S) here in all of these examples. The heterozygote males (S/s+) are visually very confusing and can appear similar to any of these phenotypes we will be discussing. Since they are not true-breeding phenotypes, they are irrelevant to this discussion). In the male, the addition of homozygous Silver (S/S) to the red duckwing creates a phenotype that would be referred to as “gold” in the hobby (image 2). The homozygous Silver changes the hackle, saddle and wing triangle to a yellow/gold color, as Aph is still present and underlies all the sex-linked pheomelanic areas, so that when the Silver gene removes the sex-linked pheomelanin the Autosomal pheomelanin is still there and is visible as the golden hue. If mahogany is present, it is also not affected by the sex-linked silver gene and will still be seen on all of the usual areas of expression and will make the tone of the gold in the sex-linked pheomelanic areas somewhat darker than if mahogany is not present. 

Image 2 - the basic red duckwing combination when the s-allele s+ is replaced with S, but no other modifications are made

In the case where mahogany is not present, all the areas where mahogany is usually seen will express as an orange/peach/golden tone that is several shades darker than the hackle/saddle shades. In the female, when we add S to replace s+, the hackle is changed to a creamy white shade while the rest of the bird remains very similar to the red duckwing hen. The major factor that will be visually different is that the back will be a cooler shade with a gray/gold tone rather than the more warm brown of the red duckwing hen. This hen is the “golden”/”golden duckwing” standard type hen as found in the standard description for that variety, such as in Modern Game. If the hen is expressing mahogany, it will be visible on the head, around the hackle and will darken the back and breast to a more reddish tone. This phenotype, in both males and females can easily be confused with both Diluted and Cream forms of red duckwing.

     So how then do we get to a clean silver duckwing phenotype? The key is to remove (or inhibit) the Autosomal pheomelanin. In my earliest research with Autosomal pheomelanin, I believed that we had a simple pair of alleles at one locus and I called those Ap and ap+ (the + being applied to the absence of Autosomal pheomelanin as I felt it also derives from a wild source – the gray jungle fowl, just as the yellow skin gene in domestic fowl has been shown to derive). However, subsequent research and test matings have shown that these two factors are not alleles of one locus. They are in fact two separate factors and are non-allelic. As I described in the April 2011 Exhibition Poultry article, I now use the abbreviation Aph for Autosomal pheomelanin. In addition, since the inhibitor of Autosomal pheomelanin is not an allele of Aph, I am now using the abbreviation Aph^I (Inhibitor of Autosomal Pheomelanin).

     So once we have replaced red (s+) with Silver (S) we find that we still do not have a true silver duckwing, so we add Aph^I to inhibit the Autosomal pheomelanin. With only one dose of Aph^I (image 3), we see only partial inhibition of Autosomal pheomelanin. The heterozygotes for Aph^I will be lighter than the pair described above, showing a creamy, yellow/white tone in the sex-linked pheomelanic areas. In the female, the breast will show some spottiness, often with each breast feather showing a very pale pheomelanic edge. One of the most interesting aspects of Aph^I is that since mahogany only expresses on Aph, when Aph^I is present, the expression of mahogany is also suppressed. Thus, in cases where there is one dose of Aph^I, even when there is homozygosity for mahogany, very little expression of mahogany will be seen in the phenotype. The most prominent expression of mahogany will be on the male shoulder/back and the female shoulder/back and breast.  

Image 3 - When there is heterozygosity for the inhibitor of autosomal pheomelamnin (Aph^I), the phenotype is lighter and mahogany has far less expression

However, when even one dose of Aph^I is present, the mahogany expression will never be solid, and will only be spotty showing several shades of orange/red/mahogany. Two doses of Aph^I will nearly completely suppress the mahogany, so that only a tiny amount is seen at the edge of the shoulder/back area of the male. (I suspect there may be at least two alleles of Aph^I, as there is some evidence that a second form allows expression of Aph and mahogany in females, but suppresses it in males. Certain lines of gray Dorking in England, for instance, seem to attest to this but I have not had any examples to test mate or observe to date. It seems this alternate allele of Aph^I allows for clean silver males and Aph expressing females. In this regard, this allele of the inhibitor seems to show sex-expression of autosomal pheomelanin, with female expression and male inhibition. I hope to comment on this seemingly alternate allele after I have studied and test-mated it further in a future article.)

     In instances where there is one dose of Aph^I, but no mahogany, we see the phenotype in the male that is called “golden”/”golden duckwing”, as in the standard description of the Modern Game variety. The standard description calls for this phenotype of male, but the female called for in that standard form is the non-mahogany form described above in the previous section. The male of this type has a yellow/cream hackle, saddle and wing triangle while the shoulder is a darker yellow-gold to pale orange-yellow. Ironically, it is the female of this type, a heterozygote, that is the standard ‘silver”/”silver duckwing” hen. She has a gray back with a slight cream tint (silver pheomelanin with black/eumelanic stippling of any size appears visually gray and layered over a small amount of Aph, there is a creamy effect), the hackle pheomelanin is white/near white and the breast is salmon, generally with a paler lace of cream pheomelanin at the edge of the breast feathers.

     The true, fully silver phenotype (image 4) is very rare, because the female is not a recognized variety of any kind and most people, upon seeing one for the first time, think she is some type of Columbian or Ginger heterozygote. These hens are rather startling if you have never seen one, as the breast is extremely pale, almost completely silver, with almost no salmon expression at all. She also has no warm tones at all in any area of her feathering. When these hens do turn up in most breeding programs, they tend to be culled out as they are generally undescribed and non-standard. 

Image 4 - the fully clean, "white" silver phenotype seen with full, homozygous inhibition of Autosomal pheomelanin

Of course, the few people in the know make full use of these hens and they produce the cleanest white, Silver males. Silver/Silver duckwing has always been a double-mated variety, however, few breeders have ever known that and cull out the proper females. This knowledge has long been a carefully guarded “trade secret”. The ironic thing is that breeders of Silver varieties are constantly complaining about “brassy” silver males, yet they routinely cull out the females that could produce the proper males. The true Silver phenotype is homozygous for Aph^I. The female is as described above and the male is simply a black and stark white combination, with all the pheomelanic areas, both Autosomal and sex-linked, reduced to white. In many instances, these males show a small amount of white at the upper breast and may show a few spots of white in the lower breast.

     In addition to the presence of S, Aph^I and mh+, most silver varieties I have test mated also carry dilute (Di) and/or cream (ig). I am not sure that either of these genes is actually necessary to get clean silver, but they certainly don’t hurt, either. Any diluter gene is only going to help remove brassiness from the silver areas. The presence of these diluters should come as no surprise. These varieties were developed long before genetic knowledge, so it only makes sense from a visual perspective that those breeders would have used any pale pheomelanic birds in their efforts to breed silver, just as any diluters and whitening genes were used in the development of solid white birds (which are known to often carry many dilution factors in addition to the major whitening gene; recessive (c) or dominant (I)).

     As you can see from this discussion, the Silver varieties are much more complicated than the simple addition of the sex-linked pheomelanic allele Silver (S) to a given red variety. This discussion applies to any silver form of any variety. That means that all silver varieties, if they are clean, true white-silver combine homozygous Silver, homozygous Inhibitor of Autosomal pheomelanin and homozygosity for the absence of mahogany and may often also incorporate Dilute and/or cream, in addition to the other genes required to make the given variety. For those comfortable with using gene abbreviations, the genes of silver are S/S (S/~ in females), Aph^I/Aph^I, mh+/mh+ and often Di/- and/or ig/ig.