DuxorW
Derailer of Threads
I previously wrote this in a ball python forum, but thought it might interest people here.
I am assuming a basic familiarity with how the banana inheritance pattern works, but if you are not familiar here is a quick review. The banana mutation is incomplete dominant. A female banana, when mated to a wt male, will produce a 1:1:1:1 ratio of male bananas, male wt, female bananas, and female wt. However, the male banana offspring of a female banana exhibit a peculiar trait. When one of these male bananas is mated to a female wt, generally all the banana offspring will be female and all the wt offspring will be male. These male bananas that only produce female bananas are called "female-makers" Rarely, a female-maker male will produce a male banana, roughly 10% of the time or less. These rare male banana offspring of a female-maker will almost always only produce male bananas when mated to a female wt. They are termed "male-makers."
A good theory of the inheritance of banana will need to explain a few observations.
1) The skewed sex ratio of banana offspring vs normal offspring when a male banana is mated to a wt female
2) Why are there male-makers AND female-makers
3) Why do female bananas seem to produce both male and female banana offspring
4) Why are the banana sons of banana females female-makers
5) Why do the rare males produced by female-makers turn out to be male-makers, unlike their fathers.
It is accepted that, like other snake species, boa/python males are ZZ (termed the homogametic sex because all the sperm contain the same sex chromosome, the Z) and females are ZW (heterogametic). However, the sex chromosomes of boas and pythons are homomorphic, meaning they look the same in a karyotype, so they can't be distinguished visually like the Z and W of something like a corn snake. It seems that it has simply been assumed that male ball pythons are ZZ and females are ZW, which is a logical assumption when there is no reason to think otherwise. There was a paper published that showed the sex chromosomes could be distinguished in the Dumerils boa because of a pericentric 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 higher-level snakes results in male offspring only, (presumably the ZZ offspring are viable whereas the WW fail to develop properly, likely because of lack of essential genes present on the Z but not the W in these species). However, in boas and pythons, parthenogenesis only results in female offspring. Because the Z and W chromosomes are indistinguishable at the morphological level in boas/pythons, you would expect boas/pythons to be able to produce both male and female offspring, or at least male offspring, by parthenogenesis if the females are ZW, as in other species. However, only females have been produced by multiple instances of parthenogenesis. There is no obvious reason why males shouldn't have been produced in at least one instance. For example, in one instance, the female offspring produced by parthenogenesis in a boa costrictor were homozygous at all loci. This means that they would have to be WW, since if they were ZW they wouldn't be homozygous at all loci, since the Z and W are homomorphic and presumably share almost all loci except whatever locus/loci determine sex. I'll come back this later.
Just go out on a limb for a moment and suppose that, 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. Technically I am saying they use an XY system since that is the designation when the female is the homogametic sex, but I am not saying the XY chromosomes are the same as in mammals, I am saying they are the same chromosomes as the designated Z and W, just that it is the female that is the heterogametic sex. I'll stick to Z and W for the sake of readers. Basically, 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 breeding results at face value in order to simplify the discussion. A male-maker is a male banana that produces male bananas and normal females when mated to a wild-type female, almost all of the time. A female-maker only makes female bananas and wt males (with rare exceptions) when mated to a wild-type female. Occasionally, a male-maker will give rise to a female banana, or a female-maker will give rise to a male 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 occasionally 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 Z/W chromosomes and that males are ZW. The banana male offspring of a female banana x wt pairing would have a Z chromosome (inherited from his mother) with the banana allele and his W chromosoe (inherited from his wt father) 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 this male banana has the banana allele on his Z chromosome, any time he passes down his Z (producing a female), that female offspring will be banana. Any time he passes down his W, producing a ZW male, that male offspring will not be banana. This explains the sex-linked inheritance pattern and female-makers. This 1:1 ratio of female bananas to wt males is just what we would expect if male ball pythons are ZW, females are ZZ, and the banana mutation is on the Z chromosome.
However, how does this hypothetical situation explain male-makers and the switch between female-maker and male-maker? Here we have to introduce the concept of chromosomal crossing over. Basically, during meiosis, the two members of a chromosome pair can 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. Imagine a cell destined to become a sperm in a ZW male. A sperm cell could only contain either the Z chromosome or the W chromosome (barring something like nondisjunction). If the banana allele is on the Z chromosome and the wt allele is on the W, a crossover event would cause the alleles to swap places, putting the banana mutation on the corresponding part of the W chromosome and the wt allele on the Z. 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 female-maker banana male, most gametes should have banana on the Z but a small fraction will have it on the W instead. If a ZW female-maker banana with the banana mutation on his Z chromosome manages to produce a MALE banana when paired to a wt female, this is because the banana allele had to swap with the wt allele on the W chromosome. So in the sperm that produced that male banana, the banana allele was on the W chromosome (most of his other "banana-carrying" sperm would have the banana allele on the Z). So we now have a male banana produced by a female-maker. He has the banana allele on his W chromosome unlike his female-maker father. When he mates to a ZZ wt female, only sperm carrying the W chromosome will produce bananas. Since W sperm will produce males, this banana is a male-maker, unlike his female-maker father. This explains the switch between female-maker and male-maker. The male offspring of this male-maker should also be male-makers, since they have the banana mutation on their W chromosome. When a crossover occurs it will allow for rare production of a normal male or a banana female.
If females are ZZ, it makes since why a female banana can produce female and banana offspring. In this case the sex would be determined by the father because the banana female can only produce eggs with the Z chromosome. So half her eggs will carry the banana mutation, and whether the offspring produced are male or female depends on whether the egg unites with a Z or W sperm. When a banana female is mated to a wt male, on average a 1:1:1:1 ratio of male banana, male wt, female banana, and female wt should be produced. Obviously since clutch sizes are small in the ball python you would have to average the result from many clutches.
Any male bananas produced by a banana female should be female-makers because they will always inherit a Z from their mother, and since their mother was banana, if they those male offspring are banana they must have inherited a Z chromosome with banana on it. Barring a crossover during meiosis, their Z sperm will carry banana and their W sperm will carry the wt allele. Z sperm will unite with Z eggs to produce female bananas, hence the banana sons of banana females should be male-makers.
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. Rare male bananas produced by female-maker sires should be male-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 the switch between them, 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 in structure in other snake lineages that there was a different mechanism for sex determination in snakes with homomorphic chromosomes. The homogametic and heterogametic sexes have changed in other lineages, such as amphibians and other reptiles, 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 in fact ZW instead of ZZ. Under the currently prevailing idea that females are ZW, these supposedly WW females would only be able to generate more daughters, if they are fertile at all, because all of their eggs will be W and males are supposed to be ZZ, so only ZW offspring should be produced. 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.
Since I came up with this idea about two years ago, a prominent researcher in the field, who initially disagreed with me, has reversed his position and in a recently published review article now suggests that an XY system (the system I am proposing, I just called males ZW and females ZZ, subsitute XY and XX) better explains the results of boa/python parthenogenesis. Hopefully his lab will verify or falsify this idea in the future.
I am assuming a basic familiarity with how the banana inheritance pattern works, but if you are not familiar here is a quick review. The banana mutation is incomplete dominant. A female banana, when mated to a wt male, will produce a 1:1:1:1 ratio of male bananas, male wt, female bananas, and female wt. However, the male banana offspring of a female banana exhibit a peculiar trait. When one of these male bananas is mated to a female wt, generally all the banana offspring will be female and all the wt offspring will be male. These male bananas that only produce female bananas are called "female-makers" Rarely, a female-maker male will produce a male banana, roughly 10% of the time or less. These rare male banana offspring of a female-maker will almost always only produce male bananas when mated to a female wt. They are termed "male-makers."
A good theory of the inheritance of banana will need to explain a few observations.
1) The skewed sex ratio of banana offspring vs normal offspring when a male banana is mated to a wt female
2) Why are there male-makers AND female-makers
3) Why do female bananas seem to produce both male and female banana offspring
4) Why are the banana sons of banana females female-makers
5) Why do the rare males produced by female-makers turn out to be male-makers, unlike their fathers.
It is accepted that, like other snake species, boa/python males are ZZ (termed the homogametic sex because all the sperm contain the same sex chromosome, the Z) and females are ZW (heterogametic). However, the sex chromosomes of boas and pythons are homomorphic, meaning they look the same in a karyotype, so they can't be distinguished visually like the Z and W of something like a corn snake. It seems that it has simply been assumed that male ball pythons are ZZ and females are ZW, which is a logical assumption when there is no reason to think otherwise. There was a paper published that showed the sex chromosomes could be distinguished in the Dumerils boa because of a pericentric 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 higher-level snakes results in male offspring only, (presumably the ZZ offspring are viable whereas the WW fail to develop properly, likely because of lack of essential genes present on the Z but not the W in these species). However, in boas and pythons, parthenogenesis only results in female offspring. Because the Z and W chromosomes are indistinguishable at the morphological level in boas/pythons, you would expect boas/pythons to be able to produce both male and female offspring, or at least male offspring, by parthenogenesis if the females are ZW, as in other species. However, only females have been produced by multiple instances of parthenogenesis. There is no obvious reason why males shouldn't have been produced in at least one instance. For example, in one instance, the female offspring produced by parthenogenesis in a boa costrictor were homozygous at all loci. This means that they would have to be WW, since if they were ZW they wouldn't be homozygous at all loci, since the Z and W are homomorphic and presumably share almost all loci except whatever locus/loci determine sex. I'll come back this later.
Just go out on a limb for a moment and suppose that, 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. Technically I am saying they use an XY system since that is the designation when the female is the homogametic sex, but I am not saying the XY chromosomes are the same as in mammals, I am saying they are the same chromosomes as the designated Z and W, just that it is the female that is the heterogametic sex. I'll stick to Z and W for the sake of readers. Basically, 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 breeding results at face value in order to simplify the discussion. A male-maker is a male banana that produces male bananas and normal females when mated to a wild-type female, almost all of the time. A female-maker only makes female bananas and wt males (with rare exceptions) when mated to a wild-type female. Occasionally, a male-maker will give rise to a female banana, or a female-maker will give rise to a male 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 occasionally 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 Z/W chromosomes and that males are ZW. The banana male offspring of a female banana x wt pairing would have a Z chromosome (inherited from his mother) with the banana allele and his W chromosoe (inherited from his wt father) 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 this male banana has the banana allele on his Z chromosome, any time he passes down his Z (producing a female), that female offspring will be banana. Any time he passes down his W, producing a ZW male, that male offspring will not be banana. This explains the sex-linked inheritance pattern and female-makers. This 1:1 ratio of female bananas to wt males is just what we would expect if male ball pythons are ZW, females are ZZ, and the banana mutation is on the Z chromosome.
However, how does this hypothetical situation explain male-makers and the switch between female-maker and male-maker? Here we have to introduce the concept of chromosomal crossing over. Basically, during meiosis, the two members of a chromosome pair can 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. Imagine a cell destined to become a sperm in a ZW male. A sperm cell could only contain either the Z chromosome or the W chromosome (barring something like nondisjunction). If the banana allele is on the Z chromosome and the wt allele is on the W, a crossover event would cause the alleles to swap places, putting the banana mutation on the corresponding part of the W chromosome and the wt allele on the Z. 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 female-maker banana male, most gametes should have banana on the Z but a small fraction will have it on the W instead. If a ZW female-maker banana with the banana mutation on his Z chromosome manages to produce a MALE banana when paired to a wt female, this is because the banana allele had to swap with the wt allele on the W chromosome. So in the sperm that produced that male banana, the banana allele was on the W chromosome (most of his other "banana-carrying" sperm would have the banana allele on the Z). So we now have a male banana produced by a female-maker. He has the banana allele on his W chromosome unlike his female-maker father. When he mates to a ZZ wt female, only sperm carrying the W chromosome will produce bananas. Since W sperm will produce males, this banana is a male-maker, unlike his female-maker father. This explains the switch between female-maker and male-maker. The male offspring of this male-maker should also be male-makers, since they have the banana mutation on their W chromosome. When a crossover occurs it will allow for rare production of a normal male or a banana female.
If females are ZZ, it makes since why a female banana can produce female and banana offspring. In this case the sex would be determined by the father because the banana female can only produce eggs with the Z chromosome. So half her eggs will carry the banana mutation, and whether the offspring produced are male or female depends on whether the egg unites with a Z or W sperm. When a banana female is mated to a wt male, on average a 1:1:1:1 ratio of male banana, male wt, female banana, and female wt should be produced. Obviously since clutch sizes are small in the ball python you would have to average the result from many clutches.
Any male bananas produced by a banana female should be female-makers because they will always inherit a Z from their mother, and since their mother was banana, if they those male offspring are banana they must have inherited a Z chromosome with banana on it. Barring a crossover during meiosis, their Z sperm will carry banana and their W sperm will carry the wt allele. Z sperm will unite with Z eggs to produce female bananas, hence the banana sons of banana females should be male-makers.
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. Rare male bananas produced by female-maker sires should be male-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 the switch between them, 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 in structure in other snake lineages that there was a different mechanism for sex determination in snakes with homomorphic chromosomes. The homogametic and heterogametic sexes have changed in other lineages, such as amphibians and other reptiles, 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 in fact ZW instead of ZZ. Under the currently prevailing idea that females are ZW, these supposedly WW females would only be able to generate more daughters, if they are fertile at all, because all of their eggs will be W and males are supposed to be ZZ, so only ZW offspring should be produced. 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.
Since I came up with this idea about two years ago, a prominent researcher in the field, who initially disagreed with me, has reversed his position and in a recently published review article now suggests that an XY system (the system I am proposing, I just called males ZW and females ZZ, subsitute XY and XX) better explains the results of boa/python parthenogenesis. Hopefully his lab will verify or falsify this idea in the future.
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