Potential explanation for banana inheritance pattern

[DRW_Reptiles]

I realize this has been discussed in depth (with no resolution) but I would like to explain a hypothetical scenario that could explain the inheritance pattern of the banana trait.

In all snakes that have hetermorphic sex chromosomes (ie, the sex chromosomes can be visually distinguished in a karyotype), females are ZW and males are ZZ. However, boas and pythons have homomorphic sex chromosomes, meaning that the Z and W chromosomes appear identical and cannot be distinguished by karyotype. As far as I can tell, it has been merely assumed that female boas/pythons are ZW and males are ZZ. There was a paper published that showed the sex chromosomes could be distinguished in the Dumerils boa because of an inversion within one of the sex chromosomes. However, the samples were taken from unsexed boas, and it appears that it was simply assumed that animals carrying one sex chromosome with the inversion and one without the inversion were female. However, as far as I am aware, there is no direct evidence that male pythons are ZZ and females are ZW.

Interestingly, parthenogenesis (reproduction without males) in other snake lineages has resulted in both male and female offspring. This is what you would expect since females have both types of sex chromosome. However, in boas and pythons, parthenogenesis only results in female offspring. You would expect boas/pythons to be able to produce both male and female offspring by parthenogenesis if the females are ZW, as in other species. However, only females have been produced by multiple instances of parthenogenesis. There are mechanisms to explain this that rely on certain events during meiosis, but there is no obvious reason why males shouldn't have been produced in at least one instance.

What if in boas/pythons, females are actually ZZ and males are ZW? This is not the simplest explanation but boas/pythons are an ancient lineage and their sex chromosomes are homomorphic, unlike other groups such as colubrids, and it is possible they have a different mechanism of sex-determination. Let me emphasize that I am NOT saying males are XY and females are XX like in mammals. We know what ancestral chromosomes the X and Y evolved from so it is impossible that ball pythons use this system. I am just supposing that in ball pythons (and other boas/pythons), the male is the heterogametic sex (produces two types of gametes, one carrying a Z and another carrying the W) and females are the homogametic sex (all eggs produced carry the Z chromosome).

This brings us back to the banana mutation. We have all heard the term "male-maker" and "female-maker." I'm just going to take some breeders results at face value in order to simplify the discussion. A male-maker is a male banana that only produces male bananas when mated to a wild-type female. A female-maker only makes female bananas when mated to a wild-type female. Moreover, it appears that in most cases when a male-maker is bred to a wt female, all (with rare exceptions) male offspring are banana and all female offspring are wild type. Occasionally, a male-maker will give rise to a female banana. It appears that female bananas are, on average, able to make both male and female bananas with equal frequency when mated to a wild type male. However, when a female-maker male occassionally produces a male banana when mated to a wt female, it seems that the male banana produced is now a male-maker, in contrast to his female-maker father. The males produced from female bananas seem to be female-makers.

The hypothesis (which I have no evidence for outside of its explanatory power, I just think it is fun to consider) that males are ZW (instead of ZZ) and females are ZZ (instead of ZW) can explain all of these observations. Lets assume that the Banana mutation is on the W chromosome. A banana male would have a W chromosome with the banana allele and the Z would have the wild type allele (I am assuming the banana locus is on both the Z and W chromosomes, which will be important later. This makes sense because the Z and W chromosome are homomorphic and should share almost all loci). Note that in this alternative scenario the sex of the offspring is determined by what chromosome is inherited from the sire. If the sire passes on a Z, he produces a female (since the female ALWAYS passes down a Z, since she has no W). If the sire passes on his W, he produces a male. Because a male banana has the banana allele on his W chromosome, any time he passes down his W (producing a male), that male offspring will be banana. Any time he passes down his Z, producing a ZZ female, that female offspring will not be banana. Thus, this theory explains both the sex-linked inheritance pattern and why male-makers exist. This 1:1 ratio of male bananas to wt females is what we would expect.

However, how does this theory explain female-makers and the existence of banana females? Here we have to introduce the concept of chromosomal crossing over. Basically, during meiosis, the two members of a chromosome pair up and swap corresponding portions of DNA. This increases the genetic variability of the gametes produced. I suggest you google it to understand it further. In the context of the banana mutation, consider what happens when crossing over happens at the banana locus in a ZW male. Consider a cell destined to become a sperm in a ZW male. If the banana allele is on the W chromosome and the wt allele is on the Z, a crossover event would cause the alleles to swap places, putting the banana mutation on the corresponding part of the Z chromosome and the wt allele on the W. There are different factors that effect how often crossover occurs. The closer two different loci are on the same chromosome, the less likely a crossover event will occur between them. Suppose the banana locus is close to the locus that determines sex. If they are close enough together but not too close, a crossover event can occur between them but only rarely.

Thus in a male-maker banana, most gametes should have banana on the W but a small fraction will have it on the Z instead. If a ZW male banana with the banana mutation on his W chromosome manages to produce a FEMALE banana when paired to a wt female, this is because the banana allele had to swap with the wt allele on the Z chromosome. So in the sperm that produced that female banana, the banana allele was on the Z chromosome (most of his other sperm would have the banana allele on the W). So we now have a female banana. She has the banana allele on one of her Z chromosomes but not the other. When she is mated to a wt male, half the offspring should be banana. But since the male determines the sex of the offspring at random, mating this female banana to a wt male should produce, on average, a 1:1:1:1 ratio of male banana, male wt, female banana, and female wt. Obviously since clutch sizes are small in the ball python you would have to average the result from many clutches.

Now we have explained the existence of female bananas. This will quickly lead to an explanation for female makers. Any male banana produced by a banana female will have the banana allele on his Z chromosome and not the W, since he can only inherit a Z from his mother. This presence of the banana mutation on the Z chromosome instead of the W will make him a female-maker. Any sperm carrying Z will produce a female, and since the Z chromosome carries the banana allele in this male, all female offspring will be banana. All sperm carrying the W will give rise to wt males. A rare crossover in this "Z Banana" male that puts the banana allele on the W chromosome of an occasional sperm will create a banana male. This "W banana" male will be a male maker, unlike his female-maker father.

To summarize, in this hypothetical scenario males are ZW and females are ZZ. A male carrying the banana allele on his Z chromosome will be a female maker. A male carrying the banana allele on his W chromosome will be a male maker. Crossing over can occasionally "swap" the banana allele from Z to W or vice versa in the gametes of a ZW banana male. Female bananas can produce male and female banana offspring when mated to a wt male, but their male offspring should be female makers.

I'm not saying this explanation is true, just that it would explain the sex-linked pattern, the existence of male/female makers, and why females can produce male/female bananas. I just am not aware of any proof that in this lineage the males are ZZ and females ZW. It appears to just have been assumed based on those snakes that have heteromorphic sex chromosomes. But it does not seem implausible that before the sex chromosomes diverged that there was a different mechanism for sex determination in snakes with homomorphic chromosomes. The homogametic and heterogametic sexes have changed in other lineages, so this would not be a first. Hopefully sequencing the genome of KNOWN males and females will shed light on this fascinating question.

(This idea makes further predictions. One is that the "WW" females produced by one instance of parthenogenesis in boa constrictor are actually ZZ females and should be able to produce male and female offspring if the males are ZW. Under the current idea that females are ZW, these supposedly WW females would only be able to generate more daughters, if they are fertile at all. Also, since apparently the sex chromosomes can be distinguished in the Dumerils boa by a small inversion, doing karyotypes with proven males and females should show that it is actually males that are heterogametic, not females.)