Dossier Mottle

By Dirk Van den Abeele

A not everyday mutation in psittaciformes is for sure the mottle. The mottle, aka progressive pied, can be found in some agapornis species on a regular basis.

There are reports of mottle personatus, fischeri, nigrigenis and roseicollis. Typical for mottle is that most birds develop the normal colour after hatching and not until after some time display a pied pattern and not infrequently, through the years, a complete yellow plumage. In other words, a mutation, which affects the available melanocytes progressively expanding the pied pattern.

It is hard to say whether this mutation inherits sex-linked, autosomal recessive or dominant. The inheritance is certainly not "mendelian" which makes it difficult to label it. It is probably one of the reasons why certain breeders do not designate it as a mutation. Also its manifestation is continually different.

In some birds a specific pied pattern develops in time, others stick to some pied feathers. Again others are considered mottle, however, all offspring appears to be normal and sometimes mottles pop up from apparently normal green birds. To put it briefly, confusion and enough questions.

Pied?

First question is for sure whether we can compare mottle with other existing types of pied, namely recessive and dominant pied. In these types of pied the eumelanin is affected in several areas randomly spread all over the plumage.

In mottles we have a randomly pied pattern so far, but if we compare the mottle with other types of pied, we see that this mutant has quite some remarkable differences. In the first place dominant and recessive pied birds hatch with a completely "developed" pied pattern in contrast to the mottle of which most specimens hatch with a normal plumage. Not until some time the pied pattern will develop and expand.

In fischeri and roseicollis we see a reduction of the mask. The cause of this is not related to the reduction of eumelanin but will probably be determined by modifying action of the genes responsible for piedness. In the mottle the mask stays unaffected.

Recessive pied is considered as ADM pied (Anti Dimorphic) in other words, recessive pied affects sex dimorphism (the physical differences between male and female individuals that arise as a consequence of sexual maturation) seen in e.g. budgerigars as the blue colour of the cere in recessive pied males turns into pink.

This phenomenon has never been seen in mottles. There are even more differences to be found if we compare the causes of normal pied and mottle. In order to understand this, it is important to know how dominant and recessive pied originate and particularly how the production of eumelanin works. I will list all these points for you.

Eumelanogenesis in the wildtype.

In wildtype agapornisses the majority of the plumage is green coloured. These green coloured feathers develop by a combined action of the available eumelanin in the medulla of the feathers (the core), the spongy zone and the yellow psittacofulvins (psittacine) in the cortex (exterior of the feather). Because there is black eumelanin in the medulla of the feather, the daylight is absorpt there and through interference in the spongy zone, blue light is omitted.

Blue light in combination with yellow psittacofulvin makes a visual green colour.

Pied birds

In pied mutants we observe a lack of eumelanin in different feather areas. Through the lack of eumelanin in the medulla, no light is absorpt. No absorption means no interference in the spongy zone, thus no blue light and all that is left is the yellow colour in the feather. That is why a pied bird has yellow spots on a green backround.

The reason why eumelanin has disappeared in pied birds must be found in the distribution of melanocytes (pigment cells). To understand how melanocytes work, we must have a look at the production process of the eumelanin granules first.

Eumelanogenesis

Eumelanin production can be subdivided into three major phases. In the skin of our birds, cells are responsible for the production of eumelanin and/or phaeomelanin. (in psittaciformes only eumelanin is produced, finch-like birds are able to produce phaeomelanin).

These cells are called melanocytes or pigment cells. These cells produce the matrices of the pigment granules at first. One must imagine these matrices as colourless almost invisible granules, in other words, the skeleton of the final eumelanin granule. These colourless matrices are composed out of at least four different proteins.

When these uncoloured matrices are complete, the first phase of the production process is finished. After that a chemical reaction starts through a certain enzyme. An enzyme is an agent with a specific task and in this case it has to activate a chemical reaction which eventually will colour these matrices black (pigment synthesis). That enzyme is called tyrosinase.

During this chemical reaction there are two possibilities. Eumelanin or phaeomelanin is produced. If during the conversion cysteine is added to dopaquinone (which is triggered from the feather follicle outside the melanocyte) phaeomelanin is produced instead of eumelanin.

However, this does not apply for psittaciformes and certainly not in agapornisses and therefore not of any interest here.

When the whole process runs in a normal way and in the psittacine birds black eumelanin granules are produced, the third and final step follows. The final step is the deposition of the fully developed and coloured eumelanin granules through long dendrites into the feathers.

In other words, we have three major steps in eumelanin production.

1. Production in the pigment cell (in the skin) of empty matrices.
2. Colouring of the colourless matrices into black (tyrosinase initiated process)
3. The completed, black coloured eumelanin transport to its destination.

Leucism:

Leucism has nothing to do with tyrosinase activity or the colouring of the matrices. The cause of this must be found in the development and distribution of the melanoblasts (precursors of pigment cells) itself.

During the early development of the embryo within the egg, the neural crest is modelled. The neural crest is the precursor of the spinal cord and the nerve system. From the neural crest melanoblasts and skin cell precursors migrate to their final destiny.

The cause of leucism is sometimes found in the neural crest or a defect in migration of melanoblasts towards the skin or a hostile environment of the skin itself. As a consequence certain skin areas lack melanocytes completely. If these pigment cells are not present in the skin, no melanin can be produced nor can it be deposited into feathers.

In recessive pied there is a defect in the production and distribution from the neural crest, the source of the melanoblasts, and as a consequence too few melanocytes arrive in some skin areas. Tyrosinase is unaffected but if only few melanocytes are available not enough pigment can be deposited into the feathers and the normal colour is missing.

Cross-sections of recessive pied feathers show sometimes few eumelanin granules but they are too abnormal to show any effect.

In dominant pied, on the other hand, normal amounts of melanoblasts migrate into the skin. However, certain skin areas have changed genetically in such a way that melanoblasts cannot survive and die. In cross-sections made of feathers taken from dominant pied birds, no matrices are to be found and so these feathers are "empty". We call these amelanotic areas.

Mottle

At the university of Massachusetts a strain of "mottle" chickens is developed in order to study this phenomenon. These "mottle" chickens show a progressive pied pattern just like our psittacine birds.

Research proved that this pied pattern is caused by destruction of melanocytes (pigment cells) in the feather follicles as well as in other tissues such as the choroids (blood vessel layer at the back of the eye). Melanocytes between these bloodvessels prevent the total reflection of light.

Scientists discovered that in the bloodstream of mottle chickens in contrast with non mottle chickens, melanocyte specific autoantibodies. These antibodies attack melanocytes in the skin and break them down. Normally a protection mechanism is present which can eliminate these antibodies, however, for some unknown reason this system does not work. Other scientists found a similarity with "vitiligo", a skin pigmentation desease found in humans.

The hallmark for vitiligo is that the skin shows pigmentless white areas. These pigmentless spots develop mostly during puberty, although sometimes small pigmentless skin areas are already present at birth. Most of the time they show during the summertime when the sun tans the skin and these spots stay white.

After some time, dependent from person to person, these spots will increase. On some people this will be limited, others have affected skin all over their entire body. This is also seen in most mottled birds. The damage to the eumelanin in the plumage can vary from some feather areas to almost complete reduction of eumelanin.

Some speciments already show some yellow feathers at birth, others become almost completely yellow after some months or years and again some others develop some pigmentless feather areas which scarcely expand.

Genotype:

Genetically spoken there seems to be quite a few differences between the mottle and recessive or dominant pied. The inheritance of the latter two mutations is clear and fits into the known  mendelian inheritance patterns whereas the mottle is poorly understood.

Not infrequently breeders have puzzled their heads over the question how it is possible that not a single mottle hatched amongst its offspring. Others thought that the inheritance might be dominant, because offspring of a mottle mated to a "non split" sometimes showed mottle hallmarks or some pied feathers. Again others thought that only mottle hens were to be found etc.etc.

The breeding results suggested for some time that we probably have to deal with polygenism.

In polygenisn we see that several mutated genes lay at the foundation of a mutation. If only a few of these genes are mutated, this does not have to show any effect or consequence.

The genes involved are not an essential part of one chromosome. The researchers at the university of Massachusetts have serious indications that at least four or five different chromosome pairs are involved.

Some genes behave autosomal recessive while others act as modifiers (only active when certain other genes are also mutated). This is a clear example of a multifactorial inheritance pattern. The chance that a mottle will pop up as a primary mutation in a specific genus will be exceptional. Most of the time we see mottles in species where several mutants are already present. Also in vitiligo there are indications that this phenomenon originated in the presence of several mutated genes.

In the book "Mutants" written by A. Leroi, the author states that at least four gene pairs are involved in the development of vitiligo.

If we list all these points in a logical way, we are able to explain these unpredictable breeding results. The fact that more than one gene pair is involved in the development of the mottle, makes it more difficult to predict the breeding results. If we mate a mottle to a non-mottle, there is little chance of considering all offspring as "split for mottle".

At the production of the gametes or germ cells during meioses, the parental cell goes through a set of four divisions. During these divisions the chromosomes are reduced to separate chromosomes, meaning that each gamete contains only one chromosome of the future chromosome pair of the new individual.

The chance that every "split" youngster will have the minimal of four necessary mutated genes for mottle is therefore limited. That would mean that the only more or less predictable way of breeding mottles is to breed mottle to mottle.

However, by the modifying quality of certain mutated genes, there is a chance that when they are only present at one chromosome (heterozygote) and during cell devision are not distributed to the gametes as a result of which not all necessary alleles are present to pass on the mottle qualities. It is recommended to use as much birds as possible from one bloodline to develop a mottle breeding stock. In this stock there is a better chance that the necessary mutated genes are present. If all mutated genes are present we must bear in mind the fact that the mottled pattern may differ from offspring to offspring. Dependent on the individual the immune system will fight the melanocyte specific antibodies and the result will differ from bird to bird. It is not inconceivable that possible environmental factors have their influence at the development of the mottled pattern.

As you can see, much is dependent on coincidence in the inheritance of this mutant, but we don't have to question whether the mottle is a mutation or not because it is. It is a mutation, only the hallmarks inherit in a multifactorial way. It is not as simple as we think to set up a stock of mottles.

As a showbird a symmetric as possible pattern is in demand in the proportion of 40/60%.

The question how to see the difference between mottle and other pied types in fischeri and roseicollis is simple; the mask. In mottles the mask stays unaffected in contrast with other pied mutations. In personatus and nigrigenis the difference is harder to see.

At the question whether it is sensible to breed mottles we are forced to make no reply. At first sight there are no factors indicating that this mutant is lethal or less fertile.

The question remains whether the presence of this mutation has a negative influence on other mutated genes present. Since we have to deal with an autoimmune system reaction, it is not notional that next to the production of eumelanin also other functions would be affected, however, we don't have any prove of that so far.

As long as the opposite has not been proven, we will have to wait for an 100% suitable answer to that. As ever it is a matter of time.

Dirk Van den Abeele
MUTAVI, Research & Advice Group, Ornitho-Genetics VZW.