Halfsiders, gynandromorphism and mosaics

Halfsiders, gynandromorphism and mosaics
By Dirk Van den Abeele
Ornitho-Genetics VZW
MUTAVI, Research & Advice Group

Published in BVA-International journal 2017

Halfsiders and gynandromorphs
Everyone has seen these halfsider birds, either in pictures or in real life. Some might even have been lucky to find one in a nest. I must admit, they do look remarkable. In most halfsiders we see that the left side and the right side of their body have different colours. But there are also ‘three quarter and four quarter birds’ [1, p. 104]. In these three or four different parts can be recognized.

A whim of nature is what you can basically call them and that is how they have been described for decades. This phenomenon is not limited to exotic birds, a lot of different species are known to have these halfsiders. For instance ‘halfsider lobsters’, butterflies, insects, mice and chickens have been scientifically described [2]–[10]. This phenomenon is even known in humans [11].

And then there are the gynandromorphs or gynandromorphism. This term is used in aviculture for birds which possess both male and female traits [12, p. 190]. In what is called bilateral gynandromorphism we have birds which have female traits on one side of their body and male ones on the others side. This has already been scientifically determined and examined [13] in zebra finches [Taeniopygia castanotis].

Of course these differences are really visible in birds with sex dimorphism (outward differences between males and females). In Agapornis fischeri and the other Lovebird species where there is no visible difference between the sexes, this will not be noticeable. In Agapornis canus it would for instance be clearly visible. For clarity sake, a halfsider bird is not necessarily a gynandromorph and a gynandromorph is not be definition outwardly a halfsider.

Yet many wonder what the origin is of these halfsiders and gynandromorphs. A lot of researchers have made a stab at this subject matter and they all agreed on one thing: the cause can probably be found in the fertilization and the first cell divisions. Lots of theories are available. But before we look into these it is important that we understand fertilization and the subsequent cell divisions.
Sex cells and fertilization Each cell in the bird’s body contains the genetic information and these will partially determine the phenotype. This information is neatly written into the DNA. This DNA is found in the nucleus of each (somatic) body cell and is spread over a number of chromosomes. It is important to know that these chromosomes are always present in pairs in birds. So of each chromosome there are, under normal circumstances, always two instances present.
Most birds produce sex cells during a certain period of their life. In the male these are the sperm cells and in the female egg cells. These sex cells are called gametes. Contrary to the normal (somatic) cells sex cells the gametes contain only one instance of the chromosome pair. During the fertilization a male sperm cell fuses with a female reproductive cell (egg cell) and thus the fertilized egg cell again contains two instances of each chromosome pair. In other words, out of two ‘half cells’ a whole cell is formed, a cell with complete chromosome pairs. This fertilized egg cell is then called a zygote [14].
Once this (fertilized egg cell) zygote is formed, a process begins which is called embryogenesis (development of the embryo until the fetal phase) and the zygote will start to double during what is called the cleavage, in this first phase. This is called cleavage because the cells do not grow in these first divisions, but become smaller because they are always halved and there is no plasma growth in the cells. During this cleavage the DNA is always neatly copied into the new cell.
The cleavage is the first step in the embryonic development from the zygote up to what is called the morula stage. The first division goes from a zygote (a fertilized egg cell) to 2 cells (the first cells are called blastomeres [15]). Out of these two blastomeres respectively the left and right side of the body will be formed through further cell divisions [16]. Next the division continues from 2 to 4 – 8 – 16 – 32 till 62 cells during this cleavage. According to most researchers the first cleavage phase is crucial for the existence of halfsiders or gynandromorphs. Once the cleavage is finished we call the embryo a blastula or blasto cyst and the cell division (mitosis) continues. This way new life is formed and the new genetic code is passed to each cell in the body [17].

In a fertilized cell or zygote the sex chromosomes are also present in addition to the autosomal chromosomes. The gender of the future young depends mainly on the sex chromosome passed from the parents. In birds the male sex chromosome consists of two Z chromosomes. Hence the male can only pass a Z chromosome through his sperm cells. The female on the other hand has a Z and a W chromosome and can either pass a Z chromosome or a W chromosome through her egg cell [18]. If the zygote contains two Z chromosomes a Z chromosome of the father and a Z chromosome from the mother) then the young is normally a male. If there is a Z (from the father) and a W chromosome (passed from the female) present, then the young is ZW and normally a female will develop in the egg.

For clarity sake, I again mention that this is ‘normally’ because research has already shown that the gender does not solely depend on the sex chromosome. There are autosomal chromosomes which can influence the gender identity [19], [20]. Because of the complexity of this fact we will not delve further into this topic but it is good to know what in addition to the sex chromosomes genes on the autosomal chromosomes can also determine the gender. In other words it is a bit more complex than what most of us suspect because as always exceptions make the rule.

Halfsider and gynandromorph theories in the 19th and 20th century
This is definitely not a new concept. The oldest paper on gynandromorphs which I have been able to review dates back to 1888 [21]. In it the author suggests that in gynandromorphs, after the fertilization, just after the first cell division of the zygote, an extra sperm cell enters and fuses with one of the two newly formed blastomeres.

Thomas Hunt Morgan [22] in 1905 and Leonard Doncaster [23] in 1914 thought that in gynandromorphs two sperm cells were indeed involved but they assumed that only one of them entered the nucleus of the egg cell whereas the other sperm cell developed independently in the egg cell, outside of the nucleus. Doncaster added a third possibility: the egg cell could contain two nuclei with DNA material, which can then be fertilized by two separate sperm cells. Later Morgan would establish another theory whereby he talked about elimination of a sex chromosome [24].
In this period it were mainly the aviculturists of budgerigars [Melopsittacus undulatus], who used this theory to explain their halfsiders. A common theory about halfsiders was that the cause could be found in the egg (egg cell) with two nuclei. But in a publication and a book from 1935, in which halfsider budgerigars were described by F. Crew and Rowena Lamy [25], [26] they brushed aside these explanations and tried to show that a loss of an autosomal chromosome is the foundation of halfsiders (or bicolours as they were called by them).

In 1959 Jerome & Huntsman published a paper in which they indicated that there are three hypotheses for what they themselves called halfsiders or ‘certain geyndromorphs’ [4].
The loss of a complete or part of a chromosome during one of the first cleavages. Non disjunction during this cleavage (when certain chromosomes do not separate or divide correctly during the division)

The origin of a mutation during this cleavage
As you can see they have various explanation and insights back in those days (and you can be sure that there were more which I did not mention here). At that time there was no clear distinction between halfsiders and gynandromorphs. It is striking that all these theories in some way were correct and even run parallel with the current insights.

Current insights in the 21st century
Of course the insights changed over time. The more information available, the better people could explain matters. Yet it seems that in this area not a lot of progress was made and that the older theories were simply developed further.
First conclusion: although the name halfsiders has been around for a long time, this term is now only used in aviculture and no longer in scientific publications. Here we now use the term ‘bicolour’ or ‘tetragametic chimaeras’. This last name, ‘tetragametic chimaeras’, is used both for the ‘normal halfsider’ and the gynandromorphs. Modern research techniques have provided us with the possibility to gain more insight genetically speaking into the possible cause of these ‘tetragametic chimaeras’.

Tetragametic chimaeras
According to a theory we must look for the cause of these tetragametic chimaeras in an egg cell with multiple nuclei. These would then be fertilized before or during the first cleavages. These zygotes would then assemble into one individual. In case of ‘three quarter and four quarter’ this would entail that three or four egg cells, in one egg, are fertilized, but I have found no research to corroborate this assumption.

According to some researchers, if this fusion of the fertilized egg cells occurs at a very early stage (so before or during the first cleavage) this could lead to a perfect halfsider whereby the two halves are neatly separated. Do realize that this is only visible when these are two different colours, in other words if both parent birds have different genes of a certain colour (e.g. green split blue x blue). The young could then have two different colour halves, green and blue. Of course tetragametic chimaeras could develop which have the same colour on both sides. This will probably go unnoticed.
The cause of ‘gynandromorphs’ could have the same basis. Depending on the sex chromosomes present in the nuclei of the egg cell (Z or W), the zygote could have male or female sex chromosomes [18]. If both nuclei get a different sex chromosome and if these two zygotes then fuse the bird would be a gynandromorph. Again, I am trying to explain it easily and am therefore forced to take a few shortcuts, but as stated already when determining the sex and the gender identity multiple processes and mechanisms are involved other than the sex chromosome.

Another theory states that during the first cleavage of the zygote, part of the genome is not copied in one of the cells fully. For instance the gene for the production of the psittacine could be damaged in one of both blastomeres. In other words, in this example, we would end up with a bird whereby psittacine is produced on one side of the body but not on the other, hence a green and a blue half [16]. And that this new mutation can come up in these halfsiders I have been able to experience personally when out of a line of wild type Agapornis fischeri suddenly a halfsider was born with on one side the normal green wild colour and on the other side the bird was SF misty green [27, p. 336].
However the question remains whether the mutation occurred during the cleavage or was already present in the sperm or egg cell.

As you can see, there are still a number of theories and personally I think they are all possible, for there are different halfsiders, various patterns, etc. So I do not think there is just one possible cause for halfsiders or gynandromorphs. Genetics cannot be easily put into clearly defined boxes.

Are halfsiders or gynandromorphs fertile?
For halfsiders the same question is always asked, whether they are fertile and the answer is: yes, some are fertile but definitely not all. Personal experience and information received from other breeders confirm this. Fact is that in the case of ‘bicolour’ halfsiders, their young, depending on the genome of the other parent bird, one or the other colour will be inherited. Do realize that, and I want to emphasize this, the phenomenon of halfsider in birds is definitely not a ‘mutation’ as we know it in our hobby. Buying a halfsider in the hopes of breeding halfsiders is therefore not recommended. Of the halfsiders which were not fertile I suspect that they might also be gynandromorph. But this is only a suspicion.
In a bilateral gynandromorph, whereby one half is male and the other is female, it is not always as clear whether they are fertile. And if they are fertile, the question remains whether the bird will have the necessary neural processes / stimulations to for instance entice a bird to breed, to pair, etc [13], [19], [28], [29]. In other words, it is still unclear and further research is needed.

Mosaics and mosaicism
First remark: these mosaics have nothing to do with the ‘mosaic canary’, let this be clear. We are talking about genetic mosaicism. In genetic mosaics we are dealing with individuals who, despite the fact that they came from a single zygote, have two different cells which differ genetically. So the DNA in the cells is not the same everywhere [30, p. 204], [31], [32]. Simply put, two different genomes (DNA) can be found randomly in the body’s cells.

One of the causes is called somatic mosaicism. During the cell divisions (mitosis – creation of body cells) of the blastomeres or probably rather the blasto cyst something goes wrong causing the DNA in the newly formed cell to not be the same as in the mother cell. This definitely does not occur during the first divisions, but in a later stage. This entails that this specific cell will further divide and as a result part of the DNA in the body will deviate. Since this effect occurs during the mitosis the characteristics cannot be inherited and cannot be passed onto the young.
Whether this also happens in birds is the question, although I have an inkling that this socalled ‘multi colour’ might be the result of somatic mosaicism.

In these ‘multi colour’ birds we have a combination of various colours. Contrary to pied where we only see a reduction of the eumelanin, in these we sometimes see pied, green and blue feathers mixed. So there is not only a local reduction of the eumelanin, but also of the psittacine. Because of this local psittacine reduction we get blue spots in green birds, or white spots in yellow birds and this is very special. Up until now I have had about five reports regarding the existence of these ‘multi colours’ in lovebirds.

These were about A. fischeri, A. personatus and A. roseicollis. The origin of the birds is usually nothing special and in the registered cases there were different genetic backgrounds. None of them however could explain this phenomenon. Each ‘multi colour’ bird has a different appearance, but it is typical for these phenotypes that these birds have a local reduction of both the eumelanin and the psittacine. The flight feathers usually exhibit a kind of ‘grizlle’ pattern. This results in grey/white flight feathers with black dots [27, p. 405].

Four out of these five ‘multi colours’ died at a fairly young age, but one of these birds, a female, did have offspring. None of these young exhibited signs of ‘multi colour’, nor their offspring. So this phenomenon fits somatic mosaicism. Of course all this must be examined thoroughly before drawing final conclusions.

Mosaics versus halfsiders.
I can understand that it is quite confusing and you can of course ask the question where the difference is with the ‘halfsider’? We must admit that the divide can be quite narrow and difficult to draw. According to most researchers the difference is probably the time when the ‘errors’ occur during the cell divisions. If it happens during the first divisions then the pattern might be more clearly defined and we refer to them as bicolour or halfsider, if the errors occur during a later embryonic phase then it is likely that this results in a ‘multi colour’ with a more variable colour pattern than the halfsider. Who’s to say?

In other words, the necessary research will hopefully provide the answer in time and a nice detail: Aviculture has not revealed all its mysteries yet.

Enjoy and keep up the good work!
Dirk

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