Fallow mysteries

Fallow mysteries
By Dirk Van den Abeele
Ornitho-Genetics VZW
MUTAVI, Research & Advice Group
Published BVA-International magazine February 2017
That the fallow mutations present in aviculture have not yet revealed all their secrets is not a new concept. Together with the opaline factor this is one of the mutations which does still raise a lot of questions and which must be followed and researched closely by us. Despite their significant presence in aviculture concrete information regarding breeding results of fallow mutants is still limited. The fact that these birds are very weak and can therefore only be bred on a small scale is definitely a contributing factor. Yet notices regularly come up which could provide a better insight into these colour mutations and which are worth while paying attention to.
For instance we received word from Werner van der Merve in South-Africa about trial pairings of split dun fallow Agapornis personatus with pastel. The breeding results lead us to suspect that dun fallow might be an allele of the a locus. Of course this is interesting news but keep in mind that this is still only a suspicion until proven. This suspicion is based on the fact that from these combinations two birds were born which could be considered as an intermediate colour.
Of course this raises a lot of speculation and various breeders have started to ask questions. Also the fact that in Spain people have started to doubt the authenticity of a dun fallow might be a further reason to (re) evaluate all possibilities thoroughly.
Current insights
I will not discuss how we arrived at the division and classification of these different types of fallow but you can read about it in my latest books, these cover the fallows in great detail [1, pp. 472–497], [2, pp. 270–295] and in my articles on this subject in various journals.
In an attempt to divide the fallow types among psittaciformes into groups a lot of discussions were held on an international level for several years. According to the existing international agreements the existing fallow types are currently divided into ‘bronze fallow’, ‘pale fallow’, ‘dun fallow’ and ‘ashen or smokey fallow’.

  • Bronze Fallow – a limited reduction of the eumelanin, both in the eyes and the plumage. The colour of the normally green feathers looks more laurel green, the eyes are a darker burgundy red.
  • Pale Fallow – here we have a large reduction of the eumelanin in the eyes and plumage. The overall body colour is yellow – with a light green hue, the eyes are a very bright red.
  • Dun Fallow – little eumelanin reduction in the plumage because of which the colour of the feathers is comparable to cinnamon or even pastel, but with a lot of eumelanin reduction in the eyes. As a result the eyes are a very bright red.

Personally I have my doubts about the existence of these ‘ashen fallow’ as a separate mutant, because they can only be found in the cockatiel [Nymphicus hollandicus] and the fact that this species has a different feather structure than most parakeets. Cockatiels have feathers of the general type and to compare these ‘visually’ to birds with feathers of the structural type does not seem to be ideal in my opinion. I would rather link them with bronze, pale or dun fallow types.
Bronze fallow, dun fallow and pale fallow can be found in a number of members of the genus Agapornis. One or more fallow mutants can also be found in various other parakeet species which can be explained based on this description.
Genotype fallows
All, presently, known fallow types inherit autosomal recessive. Some scientists are inclined to link these fallow mutants in birds to what they call the Oculocutaneous Albinism (OCA-gene). In mammals this gene is very active and a number of variations are already known, because of which individuals can be found with red eyes and a complete or limited damage to the melanin in the eyes and soft parts. Also the red eye colours are variable from allele to allele [3, p. 134]. Just to be perfectly clear this is a hypothesis. For the known SL ino types in birds proof has already been found that these are mainly linked to the MATP gene [4] and for the NSL ino types to what they call the a locus [5], [6]. Of course this does not exclude the presence of an OCA gene in birds.

Bronze fallow
In lovebirds these can be found in Agapornis roseicollis, Agapornis taranta and Agapornis fischeri.

Within MUTAVI the feathers of this mutations were studied on numerous occasions and it was discovered that this mutation, just like the NSL ino, is a type of tyrosinase negative (Tyr-neg) albinism. Whereas in NSL ino the tyrosinase activity is completely missing, in bronze fallow the tyrosinase activity is only partially reduced. This could indicate that bronze fallow is possibly an allele of the a locus. In Neophema elegans (elegant parakeet) bronze fallows are regularly cross bred with NSL ino resulting in exclusively intermediate coloured fallows with red eyes. These birds are incorrectly called ‘lace wings’ in the Netherlands and Belgium.
Another indication that this bronze fallow is probably an allele of the a locus can be found in the eye pigmentation. In MUTAVI the eyes of bronze fallow Neophema elegans and the corresponding topaz mutation in canaries [Serinus canaria] are studied. This topaz in canaries is an allele of the phaeo mutation and for clarity sake this phaeo is the equivalent of the NSL ino (a locus) in Psittaciformes. In both cases the same visible eumelanin of bad quality is present in the retina and also in the iris. This is the reason why a bronze fallow has burgundy red eyes. The a locus clearly affects the activity of the tyrosinase and this is caused by a point mutation (change within one gene, are also called Single Nucleotide Polymorphisms or SNPs) which can possibly result in a different gene defect in each bird species. It is however important to keep in mind that the tissue which makes up the front of the iris, is not the same in each bird species and that this could possible lead to colour deviations in the eye.
For this reason we were advised to represent the symbol for this mutant as an allele of the a locus (especially because this was already the case in canaries). This provides researchers with a better overview of the possible method of inheritance. If it should later turn out that these inherit differently in Psittaciformes then the symbol can simply be modified in parakeets.
No contradicting evidence has been found so far. Yet we must add for completeness sake that Mr Harry Bens performed a trial pairing about two years ago with a bronze fallow Agapornis roseicollis and an NSL ino green Agapornis fischeri. Only one young turned out to be viable, but it was green. This could be an indication that bronze fallow and NSL ino are not alleles but in these combinations this is definitely not conclusive evidence, for the mutation is located on an autosomal chromosome and nothing can guarantee that this mutation is located on precisely the same chromosome in each (separate) species. This is different in SL mutations. With these there is more certainty since most birds only have one pair of sex chromosomes.
The owners of bronze fallow Agapornis fischeri were asked to set up trial pairings between a bronze fallow and a mutant of the a locus (dec, pastel of NSL ino), but either none of the young were viable and most of them died in the egg of they refused (understandably so). According to one breeder the young from this combination had red eyes in the egg. But this is only an indication because the eye colour further developes during the first few days after hatching.
Pale fallow
Within the Agapornis genus these can be found in Agapornis roseicollis, Agapornis taranta and Agapornis fischeri. We know with a great degree of certainty that this mutation has nothing to do with bronze fallow. Harry Bens, who regularly conducts trial pairings for Ornitho-Genetics VZW, has on our request paired a bronze fallow Agapornis roseicollis with a pale fallow Agapornis roseicollis a few years ago and all young were of the wild type. In other words, a reliable result which states that these types are controlled by separate genes.

Dun fallow
The first dun fallows within the Agapornis genus originated years ago in the US in a colony of Agapornis personatus. Through transmutation (genetic introgression) this mutation was transferred to Agapornis fischeri. Despite the intense efforts by a lot of experienced breeders these fallows turned out to be a tough nut to crack. The birds are very weak and the breeding results are very limited. The preservation of this mutation is key and trial pairings are not yet up for discussion, until fairly recently …

A few months ago a few breeders started to doubt whether dun fallow is a separate mutation or simply a pale fallow. These doubts arose after darker and paler phenotypes were born within a collection of dun fallows. In principle a dun fallow has a limited eumelanin reduction in the feathers but with a bright red eye. This contrary to the bronze fallow which has a limited eumelanin reduction but a burgundy red eye. The pale fallow has a strong eumelanin reductions resulting in birds which look almost yellow with a bright red eye. In Spain Pere Carbonnell bred both paler and darker dun fallows using the same breeding pair. These paler types looked more ‘PastelIno or pale fallow like’. So it is only logical that people would start to question whether pale and dun could be one and the same mutation.
The only way to determine this is to pair both types with each other. A challenge which Johan Kip from the Netherlands, the breeder of the first dun fallow Agapornis fischeri, gladly undertook. In 2008 a dun fallow from the American line was paired with a green bird split for pale fallow. This resulted in three young, all of which were green. At the same time a pale fallow was paired with a green bird split for the (dun) fallow type from the US and three young were born from this combination. These young were also green. The number of offspring is too limited to draw any conclusions but they have us believe that this could possibly be different fallow types.
In 2009 Johan tried to pair both fallow types but this did not result in any fertilized eggs. In 2012 Johan managed to breed the first dun fallow Agapornis fischeri but this did not go down with a hitch. Let us just say that more trial pairings were bred.
A Belgian aviculturist who also had both mutations in his collection, is clearer and states that they are separate mutations. According to his statement he bred only one young from such a combination and this bird is green. He could or would not give any more information. A common problem for us.
What could be going on?
If the suspicion is correct that dun fallow is an allele of the a locus then the phenomenon in Spain can easily be explained. We could assume that the paler types are DunfallowPastels of even DunfallowDec or DunfallowInos. This could easily be tested by pairing a pastel (or NSL ino or dec) with a dun fallow. This should result in all intermediate types (DunfallowPastels or DunfallowDec or DunfallowIno’s) .

Another possibility is to pair two existing (possibly) DunfallowPastels. The expected outcome would be: a 25% probability of pastel, a 50% probability of DunfallowPastels and a 25% probability of dun fallow.
The combination of DunfallowPastels with pastel is even clearer. If we combine DunfallowPastels x pastel we get a 50% probability of pastel and a 50% probability of DunfallowPastels.
Hopefully someone will be willing to set up these trial pairings.
Further hypotheses
If, and I keep emphasizing IF, it turns out that dun fallow is indeed an allele of the a locus, then, according to the current insights, bronze fallow x dun follow should also result in an intermediate type.

Another possibility is of course that, contrary to the current assumption, the topaz mutation in canaries is not an equivalent of the bronze fallow and that this bronze fallow is therefore not an allele of the a locus. If this is the case then we must definitely modify the genetic symbol and change the names for Neophema elegans, since these results are definitely not correct.
Another hypothesis is that bronze fallow and dun fallow are one and the same mutation, but that the extra bright red eye colour and additional reduction in the feathers is controlled by the epistatic gene. In a dominant epistatic gene we see that a completely separate gene can affect a present mutation [7]–[9]. An example can be found in the common redpoll [10].
As you can see, again a number of possibilities which must all be investigated further, until then they will be only hypotheses. This keeps matters interesting as new challenges are presented. Breeders willing to help out with trial pairings are of course always welcome.
I personally hope to collect sufficient funds to help develop the Agapornis Genome Study project further, allowing us to maybe have a clear answer to these questions within a few years.
So, definitely something to look forward to and it keeps us busy (LOL).
[1] D. Van den Abeele, Lovebirds Compendium, 1ste ed. Warffum- The Netherlands: About Pets, 2016.
[2] D. Van den Abeele, Agaporniden, handboek en naslaggids – deel 2, 2013de ed., vol. 2, 2 vols. Over dieren, 2013.
[3] Lynn M Lamoureux, V. Delmas, L. Larue, en D. . Bennett, The Colors of Mice A Model Genetic Network, 1ste ed. London: Wiley-Blackwell, 2010.
[4] U. Gunnarsson e.a., “Mutations in SLC45A2 Cause Plumage Color Variation in Chicken and Japanese Quail”, Genetics, vol. 175, nr. 2, pp. 867–877, Feb. 2007.
[5] J. A. Brumbaugh, T. W. Bargar, en W. S. Oetting, “A ‘new’ allele at the C pigment locus in the fowl”, J Hered, vol. 74, nr. 5, pp. 331–336, Sep. 1983.
[6] N. Sellier, J.-P. Brillard, V. Dupuy, en M. R. Bakst, “Comparative Staging of Embryo Development in Chicken, Turkey, Duck, Goose, Guinea Fowl, and Japanese Quail Assessed from Five Hours After Fertilization Through Seventy-Two Hours of Incubation”, J APPL POULT RES, vol. 15, nr. 2, pp. 219–228, Jan. 2006.
[7] H. J. Cordell, “Epistasis: what it means, what it doesn’t mean, and statistical methods to detect it in humans”, Hum. Mol. Genet., vol. 11, nr. 20, pp. 2463–2468, Jan. 2002.
[8] J. H. Moore, “A global view of epistasis”, Nat. Genet., vol. 37, nr. 1, pp. 13–14, jan. 2005.
[9] E. T. Domyan e.a., “Epistatic and Combinatorial Effects of Pigmentary Gene Mutations in the Domestic Pigeon”, Curr. Biol., vol. 24, nr. 4, pp. 459–464, Feb. 2014.
[10] D. Van den Abeele, “FAQ: wat met de agaat barmsijs? – Dirk Van den Abeele”, Ornitho-Genetics.info, 07-jun-2016. [Online]. Available on: http://www.ornitho-genetics.info/?p=11263. [Consulted: 11-dec-2016].