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BIRD INFORMATION:
 Getting Started

General Info
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*Breeding & Genetics
     - Basic Genetics
     - Sex-Linked Mutations
     - Crossovers
     - Allelic Mutations
     - Coloration Mechanics Pt 1
     - Coloration Mechanics Pt 2
     - Genetic Calculators
     - Oddities: Tricolor Tiel
     - Oddities: The Spot Gene
     - Cockatiel Split Signs

     - Hormone Control
     - Nestboxes
     - Egg candling
     - Egg binding

Breeding & Genetics

Genetic Oddities:

the Tricolor Cockatiel

plus halfsiders and other anomalies

Note: the sex chromosomes of birds actually function according to the ZW sex-determination system and this is the terminology used by scientific sources.  It's customary in the pet-bird community to use XY terminology because it's easier to remember, and this article follows that custom.

 

A tricolor cockatiel has three colors in its plumage: grey, yellow/white (the orange cheek is lumped into this category), and a third color that typically looks like cinnamon. This color pattern looks rather simple, but the reason for it is a deep, murky mystery with no easy answers. Most cases of abnormal coloration are probably caused by a health problem or diet deficiency, but there are rare cases that appear to be caused by a genetic malfunction.  These apparent genetic anomalies are the subject of this article.  A photo gallery of tricolor cockatiels and other coloration oddities is presented below, followed by a discussion of the genetic abnormalities that may be the cause.

The photos below are numbered for easy reference. When there are multiple pictures of the same bird, each picture uses the same number with a different letter after it.  Click on the thumbnails for a larger image.  Click here to skip the photo gallery and go directly to the main text.


Bird #1A and 1B

Source: Original source, Terry Martin’s cockatiel mutations book, page 175; this scan came from Criadouro Pinheiro  (English translation here.)

Sex: Male

Known mutation genes: Possible grey pied split cinnamon “half-sider” per Terry Martin

Parents: unknown

Breeding history: produced ordinary-colored young


Bird #2A, age 25 days


Bird #2B, age 40 days


Bird #2C, age 8 months


Bird #2D as an adult

Source: Criadouro Pinheiro  (English translation here.)

Sex: Female

Known mutation genes: Whiteface pied; does not appear to be pearl; may or may not be cinnamon.

Parents: Father is whiteface split to cinnamon, pied and pearl. Mother is whiteface cinnamon split to pied

Breeding history: produced ordinary-colored young

Note the color changes on the face and back over time; the face now looks rather similar to a male

 


Bird #3

 

SourceCriadouro Pinheiro  (English translation here.)

Sex:  Unknown

Known mutation genes: Whiteface pearl pied

Parents: Unknown

Breeding history: Unknown


Bird #4A


Bird #4B


Source: ICR Facebook page

Sex: Unknown

Known mutation genes: Pied. Possible whiteface split. Will be split cinnamon pearl if male.

Parents: Father is pied split whiteface. Mother is cinnamon pearl pied

Breeding history: None (still a baby at time of posting)

This chick has paler coloring in the 'shoulder' area of the wing.


Bird #5

Source: ICR Facebook page

Sex: Unknown

Known mutation genes: Whiteface pied

Parents: Unknown

Breeding history: Unknown


Bird #6A "Jett" before molt


Bird #6B "Jett" after molt


Bird #6C "Jett" circa Sep 2013

 

Source: ICR Facebook page and NCS Facebook page. April Howes, owner

Sex: Male

Known mutation genes: Whiteface pied split lutino cinnamon pearl. Visually shows both normal gray and cinnamon markings; also seems to be showing some pearl. Any visible lutino would be indistinguishable from pied. Possible color changes over time? Hard to tell because the lighting and angle is so variable.

Parents: Mother is whiteface lutino

Breeding history: Said to produce tricolor sons. This information has not been verified and no assumptions are made about its accuracy.


Bird #7A "Picasso"


Bird #7B "Picasso"

 

Source: Bert's posts on a now-closed ICR forum.  More pictures are available at these links in Bert's Photobucket account: #1(juvenile plumage), #2(back), #3(left side), #4(right side)

Sex: Male

Known mutation genes: Pied, apparently split whiteface. Has some visible pearls in the cinnamon part of his plumage. But the cinnamon and pearl genes maybe not be configured the way one would normally expect, because the coloring of his offspring doesn't match the expected results. Odd breeding results could be due to a series of crossovers.

Parents: Father is pied split to whiteface and to pearl cinnamon yellowcheek on the same X; mother is pearl cinnamon pied.

Breeding history: No tricolor chicks. Young inherit cinnamon OR pearl, not both mutations together. His mate is lutino pied split to whiteface. The conversation at the end of this article discusses this peculiar outcome extensively.

 


Bird #8A "Mickey Mouse" as a juvenile


Bird #8B "Mickey Mouse" as an adult

 

Source: Susanne Russo’s picture album here and here and also the ICR Facebook page

Sex: Male

Known mutation genes: Creamface pied

Parents: Not reported

Breeding history: Not reported

Note the color changes over time: apparent reduction in the medium color in the center of the back, and the addition of white along the quill in some brown wing feathers. The juvenile wing coloring is easier to see in the picture for Birds #15 below.


Bird #9 "Splash"

 

Source: Susanne Russo’s cockatiel mutations e-book Sherri Tame Tiels, owner.

Sex: Not reported

Known mutation genes: Not reported

Parents: Not reported

Breeding history: Not fully reported; maternal grandmother of Bird #10 "Calico Kitty"

 


Bird #10 "Calico Kitty"

 

Source: Susanne Russo’s cockatiel mutations e-book

Sex: Female

Known mutation genes: Whiteface pied

Parents: Mother is whiteface lutino, and is the daughter of Bird #9 "Splash"

Breeding history: Not reported

 


Bird #11

Source: Terry Martin’s cockatiel mutations book, page 174

Sex: Uniform face coloring on both sides indicates male

Known mutation genes: Not reported

Parents: Not reported

Breeding history: Not reported

This bird is a quartersider who can reasonably be described as tricolor.

 


Bird #12A and B

 

Source: Terry Martin’s cockatiel mutations book, page 174

Sex: Unclear; might be a gynandromorph and/or halfsider

Known mutation genes: Whiteface pied with pearl markings on on wing but not on the other

Parents: Not reported

Breeding history: Not reported

This bird does not appear to be a tricolor. The pearled wing looks paler than the unpearled wing simply because of the white markings on the feathers.

 


Bird #13A and B


Bird #13 C and D


Bird #13E

 

Source: Wyjątkowa nimfa with further discussion at Genetics-Psittacine

Sex: Female

Known mutation genes: Can't be determined with any confidence; see discussion at Genetics Psittacine link above.

Parents: Unknown

Breeding history: Lays fertile eggs. "Passes on genotypes from both sides of her body through her gametes" which is ambiguous but probably means that some offspring resemble one side of the body and some resemble the other side.

This bird is a halfsider but should probably not be classified as a tricolor.

The location of the bird is unknown.  The pictures appeared on a Polish website but it doesn't sound like the webmaster owns the bird.

Translation of the Polish website (sorry, the Google Translator did a far from perfect job):

"I just got a picture of exceptional nymphs. It is a nymph of different colors (mutations) on each body half. This phenomenon (known in English halfsider) is quite well known in the world of birds. This looks like a parrot glued to the two separate halves. The dividing line runs through the center of the torso (when is 50/50), may also be some other aspect ratio. This parrot is a phenomenon, which is an example of mosaicism. In cultures birds of different fisheries bodies are quite common in budgies. They are also recorded in canaries, Zebra and many other species (details given Hollender 1944). Birds such it is impossible to intentionally breed (and very good), they are the result of cytological case (a bird that is the opposite of the twins), and it is not a trait inherited. This problem is not fully recognized.

"For the first time I hear about this, however, the nymph! Below pictures of females nymphs, which has sent Dr. R. Brightwell from Australia.

Clearly, the right half (pictured on our left) is yellow, while the left half is devoid of yellow dye is Caspian.""

 


Bird #14A and B

 

Source: Babu VT (owner) and Talk Cockatiels forum thread

Sex: Not reported

Known mutation genes: Pearl

Parents: Not reported

Breeding history: None

This bird has normal coloring on one side of the face and whiteface coloring on the other.  This is an example of the halfsider phenomenon that is limited to a fairly small area of the body.  This bird should probably not be classified as a tricolor.

 


Bird(s) #15

 

Source: Susanne Russo’s cockatiel mutations e-book

Bird at top left is same as Bird #8

Sex: Not reported

Known mutation genes: Not reported

Parents: Not reported

Breeding history: Not reported

The unusual coloring of these birds may have different causes. The bird on the right in particular doesn't have much in common with the other birds in the gallery except for Birds #16 below.

 


Birds(s) #16 A and B


Bird(s) #16 C and D

 

Source: Screen captures from a YouTube video. Also a discussion on the Genetics-Psittacine board

Sex: Male

Known mutation genes: Pied splits in at least some cases

Parents: Unknown

Breeding history:  several of the young males fathered offspring who did not show tricolor markings

In 2010 the owner reported 4 mature males and 6 young males entering their first molt, all with patches of brown feathers that are replaced by similar brown feathers when they molt. At the time of purchase they were being kept indoors but their prior history is unknown. The most striking individuals from the video are shown above. An update in the genetics board thread reported that the birds molted into normal coloration after several months on a good diet. But diet is not necessarily relevant; color changes over time have been observed in some tricolor birds who are still with their original breeder, and presumably on the same diet. Several theories were raised about what’s going on with the #16 flock, none of them conclusive.

A genetic cause has not been ruled out, but it seems likely that any genetic cause would be related to health/nutritional issues and the coloration would be a side effect.

 


Bird #17

 

Source: Original source, Terry Martin’s cockatiel mutations book, page 175; this scan came from Criadouro Pinheiro  (English translation here.) 

Sex: Male

Known mutation genes: Possible pearl?  The tailfeathers look grizzled and the photo quality is so poor that it's hard to tell what's happening on the body.

It seems likely that this bird is mottled/grizzled not tricolor.   

Parents: unknown

Breeding history: produced ordinary-colored young

 


Bird #18A and B

 

Source: Terry Martin’s cockatiel mutations book, page 174

Sex: Male

Known mutation genes: Not reported 

Parents: Not reported

Breeding history: Not reported

This bird has a mottled pattern that changes with every molt. Not a tricolor.

 


Bird #19 "Millie"

 

Source: Jade Katherine Rowe (owner) and NCS Facebook page

Sex: Female

Known mutation genes: Cinnamon split to pied

Parents: Not reported

Breeding history: Not reported

This bird is NOT a tricolor or a halfsider, at least not in the standard sense of the word.  Most cockatiels have darker color on the upper chest than they do on the lower belly, and in some individuals the transition is abrupt.  This bird's coloring is believed to be normal.

 

 

Minor terminology issue

Tricolor cockatiels are sometimes called Schimmel (with a variety of different spellings). "Schimmel" is a German word referring to a dapple or roan horse (one that has mottled or mixed colors on its coat). German breeder Gunter Wulf used the term to describe two of his cockatiels that had unusual plumage, and Terry Martin's cockatiel mutations book published pictures of both birds and described them as Schimmel.  However the plumage of these birds is anomalous in different ways. Bird #1 is clearly a tricolor while Bird #17 has a mottled/grizzled appearance that does not look like tricolor.  The word Schimmel is mainly used in Germany to describe a mottled/grizzled look not large patches of solid color, so it's not an ideal label for tricolor cockatiels.  But Terry Martin is the leading expert on parrot mutations and terminology, and since he used the word Schimmel to describe a tricolor it's likely that this terminology will persist.

Halfsiders

In general it appears that the tricolor phenomenon is somewhat different from the halfsider phenomenon. But it's likely that the underlying genetic cause(s) are somewhat similar and much more information is available on halfsiders than on tricolor, so a discussion of the halfsider phenomenon is warranted. 

The word halfsider describes a specific type of unusual physical appearance but doesn't indicate what made the bird look like that. The “classic” halfsider has bilateral asymmetry, meaning different colors on each side that are vertically divided more or less equally right down the middle of the bird. Some sources use the word halfsider to describe any bird with different coloring on different parts of the body that is not explained by ordinary genetic inheritance, but this tends to be confusing if the bird does not have an obvious 'half and half' division in its coloring.  Many other color distribution patterns are possible, including quartersiders who only have a partial 'split down the middle' appearance, and birds who have different types of plumage on different parts of the body that are distributed regularly or irregularly with no visible relationship to the centerline of the body.

This article will use the word halfsider to refer to birds that have a vertical 'split down the middle' appearance to some degree. Birds 11-14 in the picture gallery are clear examples of the halfsider phenomenon, and the other birds in the picture gallery are not halfsiders as defined here; only Bird #11 can reasonably be described as both a halfsider and a tricolor.  All the other birds in the gallery are one or the other or something else entirely.

There are several recorded examples of halfsiders successfully breeding but they produce normal-colored young. They breed true to whichever "side" the sperm or ovum came from. A family line of halfsiders can not be developed because the halfsider coloring is not inheritable. (Olszewski, Genetics-Psittacine)

The halfsider phenomenon has been observed in budgies (Twinzy, Houdini, budgie 3, budgie 4, budgie 5, budgie 6) and a variety of other pet parrot species including lovebirds (pic 1, pic 2, pic 3), IRNs (pic 1, pic 2), and eclectus (pic).  A 1935 study by Crew and Lamy investigated 17 cases of bicolorism in budgies, 16 of them halfsiders and all of them involving blue and green coloring. 

Page 92-93 of Terry Martin's parrot mutations book talks about halfsiders, saying "Genetically these birds are invariably Normal split blue. It is currently believed that they occur due to a genetic error as an embryo. This error deletes the Normal gene from one half of the bird, thereby allowing the Blue gene to express itself in that side of the bird." 

Parrots have two types of pigment in the body. Melanin is a black/grey/brown pigment that can be used in combination with feather structure to produce the appearance of blue. Psittacin is a different pigment which produces yellow and red colors, and when yellow psittacin is added to blue coloring it creates the appearance of green.  In essence Terry Martin's book said the halfsider phenomenon removes the psittacin pigment from part of the body. In a bird that is normally green and yellow, the part of the body with psittacin will look green and yellow and the part without psittacin will look blue and white. In species like cockatiels where the normal color is NOT green, removing the yellow will have a different visual effect. The halfsider coloring of Birds 13 and 14 obviously involves the deletion of psittacin pigment, since one side of the body has normal yellow/orange coloring and the other does not.

But in any case, the principle that Martin stated is only partly true. The coloring of most halfsiders does involve the deletion of yellow psittacin from part of the body, but there are other halfsiders where the color difference involves melanin not psittacin, including Bird #11 in the picture gallery.  The tricolor phenomenon in cockatiels is a difference in melanin coloring.

The amount of yellow coloring in a bird is controlled by the genes at the blue locus (see the article on Allelic Mutations for a full explanation of the blue locus). Color oddities that involve melanin instead of psittacin are obviously the result of something that happened to a different gene.

Tricolor observations

The picture gallery indicates that tricolor cockatiels seem to fall into two distinct categories: (1) birds with a recognizable, fairly consistent pattern where the medium tone occurs primarily on the upper wings with a fairly equal distribution on both sides, and normal (or occasionally pied) feathers in the center of the back. Birds 1-7 and are examples of this, and will be called specific-pattern birds in this article; and (2) birds with unique markings that don’t follow any specific pattern and will be called random-pattern birds. It's difficult to classify Bird #8, since his pattern has changed over time; one picture looks fairly similar to the specific pattern and the other looks random. It's probably most accurate to call him a random pattern bird. Birds 9-10 have random patterns that appear to be genetically caused. Birds 15-16 have random patterns that may or may not have a genetic cause.

Birds 11-14 are halfsiders, but only Bird 11 can reasonably be described as tricolor.  Birds 15-17 have plumage oddities that can't be described as either halfsider or tricolor, and won't be discussed further in this article.

It seems likely that the specific-pattern tricolor birds are all the result of the same genetic phenomenon, while the random-pattern birds are probably the result of different phenomena which may or may not be related to each other.

Many of the specific-pattern birds are whiteface, and most of the random-pattern birds are not whiteface. Whiteface is an alternate term for the blue gene, which is frequently involved in the halfsider phenomenon in parrots.  But there is no obvious relationship between the blue/whiteface gene and the tricolor phenomenon.

All the specific-pattern birds and some of the random-pattern birds are pied, so the tricolor phenomenon does seem to be significantly related to the pied gene. The pied gene affects the migration of melanin-producing cells in the embryo, and it appears that some of these melanin-producing cells or the DNA controlling them are "different" in tricolor birds.

Some but not all of the tricolor birds have the cinnamon gene. It isn't known how the cinnamon-like color is produced on birds that don't have the cinnamon gene. There are a variety of rare mutations that produce lighter and/or browner tones in the feathers, but none of the birds shown here are known to have these genes.

When the pearl mutation is present on a tri-color bird, the pearling doesn’t look normal. General observations of other oddities seem to indicate that the pearl gene is somewhat prone to disruption.

Tricolor birds seem to be generally capable of breeding successfully, but there are no verified cases where a tricolor parent transmitted the tricolor markings to their offspring. However there have been some observations of tricolor and other oddities within the same family. Bird #10 (Calico Kitty) is a granddaughter of Bird #9 (Splash). A son of Splash, named Ash, did not have tricolor markings but he did have a grizzle pattern to the wing spots and a moiré pattern on his wing coverts.  (Source, Susanne Russo’s cockatiel mutations e-book).

A post on the Genetics-Psittacine board here describes an example where the cinnamon sister of a tricolor male produced a tricolor baby; the uncle’s color pattern is not described but it sounds like the baby is a random-pattern bird. Two examples are not enough to conclude that random-pattern tricolor might be more reproducible than standard-pattern tricolor, but it’s a possibility. Other sources have stated that some family lines in birds are prone to producing halfsiders, chimeras, and/or genetic mosaics (discussed later).

Mixed DNA as a possible genetic cause

The prevailing opinion is that unusual mixed color patterns are caused by the presence of two or more genotypes (aka two cell lines) in the body. This terminology is clunky and inconvenient, so I'll invent my own term and call it "mixed DNA".  Normally, the body is supposed to have the exact same DNA in every cell. But in some situations a bird (or other animal) shows the colors for separate mutations on different parts of its body because it does NOT have the exact same DNA in every cell; instead there are some areas where the DNA is different. There are several ways that this can happen.

(1) With a chimera, two different zygotes fused into one individual during early embryonic development, and the popular belief is that this is where halfsiders come from. The phenomenon is the result of a developmental accident that is the opposite of identical twins - instead of one individual dividing into two, two individuals merge into one.  

However, it appears that many if not all "split down the middle" halfsiders are actually genetic mosaics (discussed below) rather than chimeras. It's said that roughly half the mammals on earth are a mosaic to some degree while chimeras are much rarer (except for a technicality involving twin cattle).  (Colorado State)

Tetragametic chimeras (the technical term for two zygotes that have blended into one individual) may or may not have visible physical abnormalities. Most chimeras look normal but may have areas of “otherness” throughout the body, where a whole organ has a different DNA type than other areas.  There may be some visible signs of chimerism, for example having eyes that are not the same color.  The visibility of the different individuals depends on how differentiated the embryos were at the time they merged, and they merge most readily at the earliest stages of development.  (Lam, The Tech)

There have been at least two cases where genetic testing concluded that human women were not the mother of their children.  The women looked normal so no one knew they were chimeras, and the part of their DNA that was tested did not come from the same "half" that the children did.  Once the chimerism was discovered and the DNA from the correct "side" was tested, they were proved to indeed be the mother.  (Project Muse)

Chimerism is not inheritable. The parent has mixed DNA but each individual cell in the parent’s body contains just one DNA type, not both.  Therefore only one of these DNA types will go into each ovum or sperm.

I can not find any clear evidence on whether or not a chimera can have the "split down the middle" halfsider appearance; some sources say yes and others say no, and none of them give an explanation for their answer. I don't know of any cases where both sides were DNA tested to give a definite answer. The sources describing a halfsider as a tetragametic chimera seem to have assumed that the individual was a chimera based on appearance.  Genetic testing is necessary to determine whether the DNA from two different individuals is present or if this is one individual with a genetic difference in part of the body.

(2) Gynandromorphs, aka intersex or hermaphrodite, occur when sex chromosome abnormalities cause the individual to have both male and female characteristics, and the female aspect dominates in some parts of the body while the male aspect dominates in others. With birds, this can cause interesting effects if the bird has one copy of a sex-linked recessive gene. The gene will be expressed in the 'female' area of the body but not in the 'male' area.

There are various causes of gynandromorphy, including (1) a chimera where two zygotes of different sex have merged, or (2) a genetic mosaic (explained in the next section) where a cell divides abnormally during early embryonic development, resulting in some cells with extra sex chromosomes;  depending on the exact mix of sex chromosomes in the local cells, some parts of the body follow the XX pattern and others follow XY. An abnormal number of sex chromosomes in a cell could theoretically be inheritable, but most gynandromorphs are sterile so it's basically a moot point.

At least one online source has stated that gynandromorphs are created in chickens when one ovum is fertilized by two sperm (National Geographic). This could certainly cause some interesting DNA effects if it was true, but I can't find any reliable source supporting the notion that such an event (polyspermy) can actually occur. Multiple sperm can penetrate the ovum in birds, but only one will fertilize the ovum and the others will soon disappear. Even if more than one sperm did fertilize the ovum somehow, it couldn't cause gynandromorphy. In birds all sperm carry the X chromosome and do not influence the sex of the zygote; it's the hen who carries the Y chromosome and determines the sex of the offspring. The misunderstood study is explained more accurately at Science Mag

(3) A genetic mosaic occurs when cells emerge within an individual with a different DNA pattern than what was originally inherited from the parents. At some point (usually during embryonic development, but it can occur later in life) there is damage, abnormal cell division, or some other spontaneous change to the DNA in one cell, and it continues to proliferate with this changed DNA. All the cells that descend from the changed cell contain this "different" DNA and behave in accordance with its instructions, while the rest of the body's cells carry the original DNA and follow its instructions. The earlier the DNA change occurs during embryonic development, the more numerous and widespread the changed cells will be.  A DNA change that occurs later in life may involve a very small area. (Wikipedia, Genetics-Psittacine)

Genetic mosaics are non-inheritable, for the same reason that chimera color patterns are non-inheritable. Each individual cell in the parent’s body contains just one DNA type, so only one DNA type will go into each ovum or sperm.

Mosaic or chimera?

I’m inclined to think that mosaicism is more likely to be involved in the tricolor phenomenon than chimerism or gynandromorphy, but there’s not enough information to rule anything out.  It’s possible that some cases of tricolor might involve one type of mixed DNA while other cases are caused by a different type of mixed DNA.

Mosaics are much more common than chimeras, and it's said that they can have a "split down the middle" halfsider appearance if the first cell division in the zygote is abnormal. If the abnormal division occurs later it can result in smaller patches of the body looking different than the rest. There's more information on the internet about gynandromorphs with this appearance than there is about halfsider mosaics, but the same principle that applies to abnormal divisions of sex chromosomes should also apply to the autosomal chromosomes.  (The Tech, Dalton State) The 1935 study of halfsider budgies by Crew and Lamy called the coloring a mosaic and assumed that abnormal division of an autosomal chromosome was involved, but this shouldn't be taken too seriously; at the time the technology didn't exist that would let them examine the DNA that closely.

Most tricolor cockatiels have patches of unusual color not a full-blown halfsider appearance. This suggests that if a mosaic is involved, the DNA change occurred sometime after the embryo's first cell division. But the color differences are extensive enough that the change was probably not too long after this point.

An article by Cryberg argues that halfsider pigeons are chimeras not mosaics. I am not convinced that this is correct however; the reasoning presents an educated opinion not a statement of fact, and the  evidence for it isn't all that solid. Unlike most other sources that say chimeras are rare, he says they are quite easy to produce. It's true that they're easy to produce in the laboratory but this uses artificial processes that would not occur in nature (New Republic).

Can these anomalies be a family trait?

Cryberg made an interesting statement about odd coloring occurring in families: "A number of people have reported lines of birds that tended to produce such chimeras regularly".   There is a similar statement on page 93 of Terry Martin's parrot mutations book: "whilst certain family lines are predisposed to producing halfsiders, it is impossible to establish them as an inherited mutation". This testimony from two different sources dealing with very different types of birds indicates that some avian family lines might be prone to genetic accidents that result in mixed DNA. However the reason for this is a mystery.

Other possible causes

It’s possible that the answer in some cases might be “none of the above”, and some factor other than mixed DNA is responsible for the third color.  All the mixed-DNA traits are non-inheritable so there may be some other explanation for the cases where tricolor seems to run in the family. The variability of tricolor patterns suggests that different examples may have different causes, and some of them might be more inheritable than others. It should be noted that the more reliable reports of multiple family members with odd plumage involve random-pattern birds, and it's more difficult to form a hypothesis about the reasons for the coloring in these birds. In some cases the coloring might be a side effect of something else that's going on in the body, such as a biochemical imbalance or an unusually high need for a particular nutrient. These conditions could be hereditary with varying levels of expression.

Unusual coloration may be caused by metabolic disorders and other illnesses, or by injury to the skin or growing feather. (Olszewski) Abnormal feather coloring can also be caused by certain nutritional deficiencies. These factors are the mostly likely cause for most cases of abnormally colored feathers, and normal coloring will usually be restored if the underlying problem is corrected. It's expected that mixed DNA will rarely be the cause when abnormal coloring is present, but there are some cases where it appears to be genetic.

As a possible explanation for the halfsider phenomenon, Pilkington suggested that physical injury to delicate embryonic tissues on one side of the neural crest could result in the subsequent daughter cells all having the same defect; in effect, a type of physical scarring proliferates across half the body.  This seems unlikely however unless DNA damage is involved.

What is the third color in a tricolor cockatiel?

It looks like the tricolor phenomenon in cockatiels mostly involves a sex-linked gene, cinnamon.  Mosaicism could easily explain the phenomenon in a split-cinnamon male, where the normal side of the gene pair was damaged and the cinnamon gene was left in sole control of melanin coloration in the local area, similar to the way that an unpaired cinnamon gene produces visual cinnamon color in a hen.  

But what about a tricolor bird who is genetically a visual cinnamon male, a male with no cinnamon genes, or any hen whether she has the cinnamon gene or not?  Some speculation from me, based on no evidence at all: in a visual cinnamon male, maybe one of the cinnamon genes breaks in a way that restores some of the normal function or otherwise prevents the undamaged cinnamon gene from taking sole control, so the feather reverts to the default normal grey coloring. Similarly, the sole cinnamon gene of a hen might be changed so the feather reverts to normal grey.

For birds with no cinnamon genes, maybe there is a change in some other gene which results in a cinnamon-looking feather that is not true cinnamon. 

If it isn’t cinnamon in some cases, then what is it?  The pied gene normally removes all melanin from a pied feather. Is it possible to have an incompletely pied feather, where only some of the melanin is removed and this reduced amount of melanin is spread evenly throughout the feather? Probably not. The pied mutation interferes with the migration of melanoblasts in the embryo. Pied feathers are the result of not having melanin-producing cells in the area, and there's no ability to put melanin in these feathers. There may be cases where there are some melanocytes in the area but not enough to color the whole feather. But it's most likely that this causes grizzled feathers (which are not uncommon in pied cockatiels), not an even distribution of diluted melanin coloring. 

There might be some other kind of dilution effect going on, with less melanin being produced in these areas. Or perhaps the amount of melanin is normal, but it's not forming properly so the color is "off". There are known mutations that have similar effects so it's conceivable that the DNA could break in a way that produces this type of coloration in a limited area. The clues still point toward mosaicism or a non-genetic cause.

Susanne Russo asked about the patch of cinnamon feathers on Bird #8 on the Genetics-Psittacine board. The response was “It could be theorised that a local gene defect in that patch of skin caused damage to the cinnamon locus and therefore that patch was unable to convert brown into normal black eumelanin.” The term “genetic mosaic” wasn’t used, but is apparently what was meant, suggesting that a bird with normal grey coloring had localized damage that prevented the melanin pigment from being processed normally.

Technical details - Migration of embryonic pigment cells

Melanoblasts (precursors to melanin-producing cells) arise from the dorsal (top/back) side of the neural crest (the precursor to the brain and spinal cord) and migrate laterally towards the ventral (front/bottom) side of the body where they meet more or less along the midline. This migration pattern explains how the halfsider 'split down the middle' appearance is created when each side of the neural crest is genetically programmed for a different color scheme.  Melanoblasts do not arise uniformly along the length of the neural tube; in general, a large pool is present in the cervical region and significantly fewer in the trunk. With piebald/pied mutations, melanoblasts form and begin to disperse but do not migrate very far, so that areas close to the point of origin are more likely to receive melanoblasts than areas that are further away.  In birds, pigment cells enter the migratory pathway at the level of the forelimb (wing), which is probably the reason that the upper wing is more likely to retain melanin coloring than any other part of the body. The migration path to the upper wing is shorter than the path to many other parts of the body, so the melanoblasts have a better chance of reaching their destination. (Parichy et al, Osawa, Genetics-Psittacine)

The mechanics of psittacin production and distribution are unknown. But based on the existence of halfsider birds where one side has psittacin pigmentation and the other side does not, it appears that the migration of psittacin-producing cells in the embryo is similar to that of melanin-producing cells.

In humans and a few other mammals, a phenomenon called “Blaschko’s lines” has been observed. This is a pattern of lines on the skin which is invisible in most individuals but may become a visible pattern of stripes or markings in chimeras/mosaics or people with certain skin diseases. It’s believed that these lines show the migration pattern of embryonic cells as the individual developed. These markings tend to be fairly symmetrical. The pattern isn't limited to 'tiger stripes' and there are a variety of other patterns that can occur including large patches of color (Medical Grapevine).  Blaschko’s lines have not been observed in birds and are not directly related to the tricolor phenomenon; however it does demonstrate that a DNA change in one cell during an early stage of development may be spread across a wide area of the body following the migration pattern of embryonic cells. (Wikipedia; also google “Blaschko’s lines” and check out the Image results for dramatic examples of how this phenomenon can manifest in humans)

More speculation on the pied gene and multiple-gene interactions

Terry Martin has hypothesized that there are 10-20 genes involved in producing pied patterns, including major genes (both dominant and recessive) that produce significant patterns, and minor genes (again, both dominant and recessive) that produce smaller patterns, as well as modifier genes that don't directly produce a pattern but have an effect on the pattern genes.

It seems to me that all these genes probably have some kind of influence on the migration of melanoblasts or perhaps on their survival, resulting in a sort of local control where some parts of the body respond to the pied gene(s) more easily than others.  The back of the head responds so easily that a pied split often causes markings there. The upper part of the wings seems to be the most resistant to the pied gene, and is the body part that is most likely to be solid grey on heavy pied birds. But this seems to be the body part that is most affected by the specific-pattern tricolor phenomenon.

Speculation on color changes over time

It seems possible that gynandromorphy might be involved in at least some cases where the bird’s color changes over time; specifically in cases where a hen experiences male-style plumage changes, or conversely in cases where a male retains female-style markings in adulthood. Since many of the examples are pied, retention of juvenile markings by males could simply be the pied mutation's typical interference with the normal sexual dimorphism. It’s also possible that a metabolic disorder or dietary deficiency was involved in the original color difference, and it got better or worse over time. Genetic factors could be involved too; there are some mutations where the coloration typically develops and changes over time.

Other info on mosaicism that probably isn’t relevant

In many mammal species, all females have a type of mosaicism caused by one X chromosome being randomly inactivated in every cell of the body; in some cells the paternal X is inactivated and in other cells it’s the maternal X. This is what causes the tabby pattern in female cats. However there is no indication that a similar phenomenon occurs in birds. (Onsman)

Conclusion

When all is said and done, we still don't know what causes this coloration.  But even though tricolor isn't inheritable, it seems likely that there is a genetic cause in at least some cases.

(end of main article)

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Supplemental info

Just for fun, here's a conversation that took place on a now-closed ICR forum, where the original version of this article was posted by the LFB webmaster. It's mainly interesting as an illustration of how difficult it is to identify what is causing the observed phenomena. However part of the discussion talks about the mechanisms that are used to repair damaged DNA, which could have a bearing on the tricolor phenomenon. The main article was subsequently updated to include new information, so it's possible that some of the following discussion is outdated now. Different-colored fonts are used below to help identify who's talking.

Bert: From time to time we also get questions about these kind of birds on our Dutch forum, for example this one: [pics A and B of Bird #7]

I agree this probably is some kind of mozaicism, like Tielfan explained. I don't think however other colour mutations have an impact on the expression of these 'special effects' (besides from their usual impact, like patterns in pied)

For example, the bird I show here is kind of 'symmetrical' (partially hidden by the pied mutation), while it is obviously not a whiteface.

These kinds of 'halfsiders' like we use to call them, never proved to be inheritable.

Tielfan: I would call this a "specific-pattern" tricolor.

Do you know anything about this bird's history? Its sex, what mutations the parents have, whether this bird has done any breeding?

Bert: Some more information:

Parents:
 Male: pied split to whiteface and cinnamon opaline yellowcheek (on the same chromosome)
Mother: cinnamon opaline pied

He retained his pattern after the juvenile moult. This bird is a male, he's fertile and has bred several chicks with a lutino female.

The chicks inherit cinnamon OR opaline, not both mutations together.

Tielfan: Quote: The chicks inherit cinnamon OR opaline, not both mutations together.

This is peculiar. He should have cinnamon opaline on the X he got from his mother. The X he got from his father could have cinnamon opaline, or no mutations, or if there was a crossover it could have just cinnamon or just opaline.

One possibility is that he inherited just the cinnamon gene from his father, and early in development the cinnamon gene on his mother's X got damaged and is nonfunctional. So part of him is cinnamon split to opaline (visible on the wings), and part of him is grey split to cinnamon on one X and to opaline on the other X. If the cells involved in reproduction only have the DNA for grey with two splits on different X's, that would go a long way toward explaining your results. But it's common to have crossovers between cinnamon and opaline, so you'd still expect to have some percentage of female chicks with both mutations. I need to think about this for a while. There might be other ways to explain your results.

A few more questions:
1. Did this male ever have any visible pearling? It might have looked abnormal, because tricolor seems to disrupt pearl at least some of the time. If there was any pearling, was it located on his grey feathers or his cinnamon feathers?
2. Is it just the female chicks who are inheriting either cinnamon or opaline, or are the male chicks doing it too? Were there any female chicks who didn't inherit either gene?
3. Is it possible that the lutino mother has the pearl gene and/or the cinnamon gene?

I really enjoy trying to figure out problems like this, so I'm glad you're interested in talking about it!

Bert: I've looked it up, chicks from this bird:
Two pieds
Three opaline pied
Three whiteface pied (one died early)
One pied cinnamon

I don't know the sexes of these chicks, as there hasn't been an update yet about this matter. I've asked the breeder about it and will let you know when I hear more. But it's rather clear that the opalines and cinnamons can't be males, as their mother doesn't have these mutations.... The female is not just lutino, but lutino pied split to whiteface.

Also the male appears to be split to whiteface. He has some pearl markings in the cinnamon part of his plumage.

Tielfan: I was hoping that he didn't have visual pearling because it really complicates the situation. I can't think of any simple explanations involving a mosaic, and the complicated explanations seem like very low probability events. I'll tell you my ideas anyway. If it's a genetic mosaic, then apparently part of him is cinnamon pearl and part of him is grey, presumably split to cinnamon pearl on the X2 and possibly split to something on the X1.

One possibility is that he is a gynandromorph (part male and part female). Every cell in his body is supposed to have two X chromosomes in it, but sometimes these cells don't divide properly so you end up with some cells that have three sex chromosomes and other cells that only have one. A cell that was supposed to divide into two cells that are X1-X2 and X1-X2 instead divides into two cells that are XXX and X0, and these cells continue to proliferate with this abnormal number of chromosomes. If the X in the X0 cells came from the mother it will have cinnamon pearl on it, and he would be visual cinnamon pearl in areas with this DNA. So that cell would be X2-0, and the cells with three X's would be X1-X1-X2 (two X's from the father and one from the mother). If he didn't inherit any sex-linked genes from dad, that would be two grey genes and one cinnamon pearl gene, and he would be grey split cinnamon pearl in areas with these chromosomes.

The biggest problem with this idea is that gynandropmorphs are usually infertile. I'm not completely sure of the reason, but it's probably because they have mixed male and female hormones that aren't balanced right for reproduction. If he could reproduce with these messed-up chromosomes, it would be possible to use crossovers to explain the babies' colors; all the female chicks came from sperm that developed from XXX cells, and in all cases a crossover had separated the cinnamon and the pearl.

Another possibility is that he inherited his father's cinnamon pearl gene, and he is supposed to be visual cinnamon pearl. But sometime during embryonic development, one of the X's was damaged so badly that both mutation genes on it became nonfunctional. The problem with this explanation is that cinnamon and pearl aren't close together on the X, and anything that would damage both of them would damage a lot of other genes too which seems like it ought to be lethal. But if it's possible to have that much chromosome damage and survive, he would be cinnamon pearl in some parts of the body and grey split to cinnamon pearl on the same X in other parts. A lot of crossovers would still be needed to have four babies who were cinnamon or pearl but not both.

Maybe the simplest explanation is that it isn't a genetic mosaic at all; instead it's an unusual multiple-gene interaction that causes his cinnamon pearl split to become visible on the wings but nowhere else on the body. The pied gene would probably be involved somehow since it causes patchy coloring on different parts of the body. You would still need a lot of crossovers to get babies who were cinnamon or pearl but not both.

Bert: One thing I don't agree on: Quote: one of the X's was damaged so badly that both mutation genes on it became nonfunctional.

Colour mutations themselves are the result of damage, in almost all cases to one single gene resulting in losing its function. This means that a colour mutation can't be 'undone' by extra damage to the same gene. Instead, it could be undone by a back-mutation.

Unfortunately, this doesn't seem to explain the colours of this bird, as a back-mutation is also rare, and would have to happen twice in this case (both for cinnamon and opaline). May I introduce another theory, following on yours I've quoted above: What if this bird is actually a male split to cinnamon and opaline on the same chromosome.

But in his embryonal stage, while cell division was happening, something odd occurred. During cell division, DNA is doubled (each chromosome is doubled) and divided over two new cells. Something went wrong, resulting in a cell that got two chromosomes with opaline and cinnamon. (So the chromosome without colour mutations was lost) This resulted in a part of his body that's opalinecinnamon (on both chromosomes), while the major part of his body is only split to opalinecinnamon.

To explain chicks receiving either cinnamon or opaline, crossing-over indeed is necessary. But as the crossing-over rate between those mutations is over 30%, this is not so extraordinary.

Furthermore, the pearl markings are not that obvious, so he could be split to opaline and cinnamon on separate chromosomes. We will never be able to find out the truth unless with expensive DNA testing. But in practically all possible theoretical cases, these kinds of patterns aren't inheritable, unfortunately.

Tielfan: Quote: Colour mutations themselves are the result of damage, in almost all cases to one single gene resulting in losing its function. This means that a colour mutation can't be 'undone' by extra damage to the same gene.

I don't know enough about genetic theory to intelligently agree or disagree with this. But it seems to me that a mutation that was inherited from a parent in the normal manner is not usually defined as a damaged gene, and is considered to be a normal variation in the genome of the species. A DNA change that occurs after conception is more typically defined as damage, and it's reasonable to say the same about a DNA change that occurs during the formation of sperm and ova, so that the offspring inherits a gene that is not part of the parent's DNA.

The back-mutation idea is as reasonable as any other idea that has been proposed so far. The probability is very low, but so is the probability of everything else that's been discussed.

Quote: Something went wrong, resulting in a cell that got two chromosomes with opaline and cinnamon. (So the chromosome without colour mutations was lost)

Or the chromosome without color mutations was not lost, and the male has some cells with two normal chromosomes in them. Most of his body has the expected X1-X2 DNA, but some areas are X1-X1 or X2-X2. This might be possible, and his whole body would be genetically male.

This gave me an idea for another gynandromorph variation, where he inherited opaline pearl on his mother's X and no mutations on his father's X. It involves the XXX and X0 messed-up split that we talked about before, but this time it's divided up as X1-0 (the father's grey X paired with nothing) and X2-X2-X1 (two copies of the mother's cinnamon pearl X combined with one copy of the father's grey X). We don't actually know what happens when two copies of a recessive gene are combined with a dominant gene. Maybe the majority rules, and if the combined cinnamon happened only in the small area of the wings that has visible cinnamon pearl, and not in numerous places throughout his body, most of his body would be genetically male and maybe his hormones would be normal enough to breed.

I have an alternate explanation for the colors of the babies, once again using the example where he inherited opaline pearl on his mother's X and no mutations on his father's X. The time that crossovers normally occur is during sperm production (meiosis). But what if a crossover happened during mitosis (the normal duplication of cells) during the father's embryonic development? He would have some cells that have cinnamon on one X and pearl on the other X, and if this was the prevailing DNA in his sperm-producing area you would expect most of the female babies to be one color but not both. I didn't know whether it was possible for this to happen so I did some research. Apparently it can happen. From Wikipedia: "In another model, two overlapping sister chromosomes form a double holiday junction at a common repeat site and are later sheared in such a way that they switch places." There's a lot more technical information available on how this works but I didn't slog through it. A crossover like this explains the babies mutations but not the cinnamon pearl patches on the father.

There's a complicated way to explain everything using crossovers. The link says that damaged DNA on one chromosome can be repaired using copied DNA from the other chromosome: "Alternatively, a crossover can occur during DNA repair if, due to extensive damage, the homologous chromosome is chosen to be the template over the sister chromatid." There are other ways that DNA can be repaired after damage occurs; the link is at Wikipedia. Once again I didn't try to slog through all the technical jargon. I did notice that it says "DNA damages and mutation are fundamentally different" and it goes into detail about how they're different. We're still using the situation where he inherited cinnamon opaline from mom and nothing from dad. Sometime during embryonic development there was some kind of environmental factor that damaged the X chromosomes in three cells, and the damage was patched with a copy of the corresponding section from the other X. Here's a picture showing what could have happened. The X's are marked with red and blue; one of these colors represents the cinnamon gene and the other one represents opaline, and plain black is normal.

It seems unlikely that the embryo could suffer this much damage and survive, but everything else we're talking about is a low-probability event and this might not be as unlikely as some. With this scenario, he could be cinnamon pearl in some areas and split to cinnamon or pearl in others.

Bert: All are possible scenarios, and most are (very) rare. Problem is that we can't prove which is the right one. Indeed crossing-over is possible during mitosis, only the rate is about 1000 times lower as crossing-over during meiosis, so again: very rare. To go further into this discussion:

Quote: But it seems to me that a mutation that was inherited from a parent in the normal manner is not usually defined as a damaged gene, and is considered to be a normal variation in the genome of the species.

Mutations are faults that occur during DNA duplication. Maybe 'damage' is word that's too strong, it could better be explained as 'alteration'.

Most colour mutations are the result of a single gene losing it's function due to alteration/damaging of the gene by mutation. Once the alteration has happened, this is inherited to offspring (50%), and they could give it to their offspring without anything odd needs to happen.

This could be illustrated by some colour mutations in which the functioning is more or less known. There's always a 'lost function' involved, for example:

SL cinnamon: lost the function to fully oxidize the molecule that forms into eumelanine, probably by lacking the enzym tyrosinase.
SL lutino: lost the function to form normal melanosomes (these carry eumelanine), most melanosomes in lutino are heavily deformed.
recessive pied: lost the function to transport melanocyt cells to parts of the skin, from where feathers are formed (melanocyt cells make melanosomes)

Tielfan: I agree, this is a better description of a color mutation.

If crossovers during mitosis are 1,000 times rarer than crossovers during meiosis, then we'd expect crossover between cinnamon and pearl during mitosis to happen once in every 30,000 birds. That's a low frequency, but there are probably hundreds of thousands of domestic cockatiels who have both genes so there will be some individuals where it happens.

I don't know the frequency of the other events that we've talked about - one in ten thousand? More? Less? There might have been more than one low-probability event that occurred in this bird, so we might be talking about odds of one in hundreds of thousands. But it's still expected to happen sometimes.

If the rate of pearl/cinnamon crossovers during meiosis is 30%, then I estimate the odds of getting four crossovers in a row as .0081 - about 1 in 124. Not a high probability, but much better than one in several thousand. I've hit a lower probability than that in my own small flock. Buster and Shodu are supposed to produce 50% whiteface babies, but their first 8 chicks were not whiteface. The odds of getting 8 in a row like that are 1 in 256. I'd decided that Buster must not be split whiteface after all when chick #9 proved that he really was.

Bert: Indeed we could calculate the possibilities for crossing-over. For cinnamon/opaline the crossing-over rate is actually 32,7%, but your calculation remains close to the correct number (1,14% or 1 on 87).

The 30% rate is for lutino/opaline crossing-over. Unfortunately these crossing-over percentages are obtained from research with budgies and lovebirds. There's more and more evidence from genetic research that cockatiel sex chromosomes could be different. But fortunately, at first sight these percentages do seem valid with breeding results with cockatiels.

As for probabilities for the other scenarios, I don't know them either. I'd be surprised if there has been research done in birds on these subjects.

Tielfan: The sex chromosomes of cockatiels might be different in more ways than just the crossover rate. Genetic mosaics in other psittacine species usually involve the blue (whiteface) locus. In cockatiels it seems to be cinnamon, or maybe it's even the pied gene behaving in some weird manner. That's a completely different chromosome, which seems very strange to me. I'm trying to ask about it on the Genetics-Psittacine yahoo group but I'm not getting responses so I don't think anyone has any insights on the situation. They're having a lively discussion about ringnecks at the moment so people are definitely paying attention to the board.

The substantive part of the conversation ended at this point.  Unfortunately the Genetics-Psittacine board shut down shortly afterward so I was never able to get an opinion from an avian genetics expert.

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