Simple Mendelian sex-linked chromosome fruit fly question

Question

From my molecular biology textbook:

When red-eyed flies (dominant) were mated with white-eyed flies (recessive), most, but not all, of the F1 progeny were red eyed. Furthermore, when the red-eyed males of the F1 generation were mated with their red-eyed sisters, they produced about one-quarter white-eyed males, but no white-eyed females. In other words, the eye color phenotype was sex-linked.

First, wouldn't recombination scramble the eye color alleles among the sex chromosomes?

Secondly, even without recombination, the F1 generation will be heterozygous and all F1 flies will have white and red alleles. Some F1 males will have a white X and some F1 females will have a white X, in which case it should be possibly to have an F2 white fly.

Can someone explain this?

Answer 1

I think the text is slightly misleading. But before going into the detail genetics of eye color let's answer your first question.

First, wouldn't recombination scramble the eye color alleles among the sex chromosomes?

Two X chromosomes do recombine but one X and one Y chromosome do not recombine (to the exception of the so-called pseudo'autosomal region).

I am not sure why recombination would change anything here. I think the eye color of flies in determined by a single locus.

How is this possible?

Let's go through the text slowly because I think the text is a little misleading. I am suggesting the only scenario I could think of that would explain the observed pattern. Note that this scenario also depends on the interpretation of the text and I would need more info on the experience to make sure my interpretation is right.

When he mated red-eyed flies (dominant) with white-eyed flies (recessive), most, but not all, of the F1 progeny were red eyed.

Actually, only males are sometimes white eyed here. And to be more accurate, if sex was uncorrelated form eye color in the parental lines, then half of the males should have white-eyed.

What was happening here is that red is dominant, white is recessive and the locus for eye color exists only on the X chromosome. As a consequence, all F1 females are now heterozygous (and display the dominant red-eyed phenotype) and all males are hemizygous, half of them having the red-eyed phenotype while the other half have the white-eyed phenotype.

Furthermore, when Morgan mated the red-eyed males of the F1 generation with their red-eyed sisters, [..]

Let's forget about the white-eyed males from above, we will just cross the red-eyed males with their sisters.

they produced about one-quarter white-eyed males, but no white-eyed females.

By they produced about one-quarter white-eyed males what is meant is that a quarter of all individuals were white-eyed males. That is half of the males were white-eyed. The other three quarters of the individuals were red-eyed.

The males received their X chromosome from their mother only (as they can only receive the Y chromosome from their father). Half of the males have therefore received the white-eyed allele while the other half have recevied the red-eyed allele. For the females, they all received from their mother either a white-eyed allele from their mother or a red-eyed allele. As we selected only father that had red eyes in the previous step, all father carry exclusively the red-eyed allele. As a consequence, all females receive a red-eyed allele from their father. Therefore half the females are homozygous red-eyed or heterozygous. In any case, all females are red-eyed.

Answer 2

In the first cross, if we talk of a single mating pair of flies, one parent is red eyed, one is white eyed. The ambiguity about sex leaves two options, 1) red eyed male crossed to white eyed female, 2) white eyed male cross to red eyed female. If it were the former (red eye male) then the mother must have two X chromosomes both of which have do not carry the dominant red eye allele, and all daughters would be red eyed and all sons white eyed (their X always comes from the mother).

If it were the latter (white eye male) that would leave two further possibilities, mothers are homo- or heterozygous for the dominant red eye allele. If the mother is homozygous for the red allele then all offspring should have red eyes, all will receive an X that carries the dominant red eye allele. If the mother is heterozygous then half of the offspring will be red eyed and half white eyed, because both of the fathers sex chromosomes do not have the red allele (the X and the Y) and only one of the mothers carries it.

In the exercise, you have some white eyed flies in the first offspring, but not all, and most are red eyed. Given the wording of the question (that red eyed flies were mated to white eyed flies, and not a red eyed fly was mated to a white eyed fly) I would suggest that the first generation was produced by crossing multiple red eyed females to multiple white eyed males, and that the females were a mixture of hetero- and homozygotes. Therefore some of the offspring were white eyed. The point being, with the first cross it is impossible to tell whether the females used were each hetero- or homozygotes, you can't deduce their genotype.

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In the second cross, both parents have red eyes. What this tells you is that the fathers have an X chromosome with the dominant red eye allele, and the mothers have at least one X with the dominant red eye allele. They produce sons and daughters, among which, 1/4 are white eyed males, and none are white eyed females. The implied/logical further outcome is then that 1/4 of the offspring were red eyed males, and 1/2 (2/4) were red eyed females. In the second cross the mothers must be heterozygous (have just one red eye carrying X chromosome). The key difference here is that you can establish the genotype of the parental flies.

The cross below shows this. The sons, who inherit an X from their mother and Y from their father, are white eyed half of the time because there is a 50% chance of inheriting a red eye X from the mother and 0% chance of inheriting a red eye X from the father. Females are always red eyed because the X comes from the father, and he has only one X (which carries the red eyed allele). Half of the daughters will be heterozygous, and half homozygous, for the red eye allele, but it is dominant so all have the red eye phenotype.

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I assume that recombination cannot occur in males (D. melanogaster has no recombination in males) and therefore has nothing to do with the solution, but that depends which species of fruit fly the example refers to - could you clarify? It appears this is this book, and therefore it is D. melanogaster.