11. The Balance Theory of Sex Determination

From: The 7 Sexes

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11 The Balance Theory of Sex Determination From 1907, when Thomas Hunt Morgan began working on fruit flies, until 1915, he and his students believed that their sex chromosome composition was 2N = 8,XX for females and 2N = 7,XO for males because they had misinterpreted a paper that Nettie Stevens wrote in 1907. Once Morgan and his students realized that Drosophila melanogaster used the XXfemaleandXYmalesystemforsexdetermination,theyhadtoreconciletheroleoftheYchromosomeinsexdetermination .1Sinceitwaswell known from Edmund B. Wilson’s and Stevens’s work that some Diptera had XO males and others had XY males, they concluded that the Y could not be playing a role in the sex determination of males. That inference was reinforced when Calvin Blackman Bridges (1889–1938) discovered a phenomenon he called nondisjunction, the topic on which he wrote his PhD dissertation, which was published in 1916.2 Bridges found an unexpected appearance of a white-eyed male in a cross that should have given red-eyed males. If one parent is a whiteeyed male and the female parent is red eyed, all the progeny should be red eyed. When Bridges tried to mate the white-eyed male, he found it was sterile. He also found that if he did a cross with a white-eyed female and red-eyed male, the offspring should be white-eyed sons and redeyed daughters: a distribution that the laboratory referred to as crisscross inheritance. But Bridges found a female that was white eyed on some occasions. That exceptional female was fertile, and when mated to a red-eyed male she gave an unusual distribution of progeny: about eight percent of the offspring being of an unexpected kind with respect to their eye color and sex. 72 The 7 Sexes AfterdiscussingthesefindingswithMorganandhisfellowstudents, Bridges concluded that in the first instance, the sterile white-eyed male arose when a sperm bearing the X chromosome containing the white alleleencounteredaneggthatlackedeitherofthetwoXchromosomes .He called this failure of the egg to have a sex chromosome nondisjunction. The sterile male produced by the nondisjunctional egg and the normal spermwasXO.ThismeanttheYdidhavearole,butitwasoneassociated with male fertility and not sex determination: something other than the Y was involved in making males. He concluded that his second exception —the white-eyed female—had received a sperm with a Y chromosome and an egg, otherwise haploid, bearing two X chromosomes that failed to separate. This produced an XXY female. What this showed to Bridges was the irrelevance of the Y chromosome in the female genome. If the XXY female was fertile, but her egg production was messed up because the Y could pair and separate from an X chromosome or the two X chromosomes could pair and separate, this would account for the unusualdistributionofoffspringhefound .But,ifeggscouldbeproducedas a secondary nondisjunction, some of them should be XX and have a fifty percent chance of being fertilized by an X bearing sperm. This should produce flies (if they are viable) with a composition of 2N +1 = 9,XXX. Such flies were found and they were female, but weak and sterile, unlike the 2N+1 white-eyed fertile females that were XXY.3 Bridges later discovered another unusual fly: a somewhat larger female that turned out to have a triploid 3N = 12,XXX chromosome composition . She was also fertile, but when crossed with diploid males she producedsomefertiletriploiddaughters,nofertiletriploidsons(actually XY with a triple set of autosomes), and a variety of diploid offspring with XX or XXX or XY or XXY sex chromosome content. The triploid or triploid-likesterilefliesthatwereXXorXXYwerenotquitefullyfemale and showed abdominal patterns that were partially male. They clearly had some sort of intersex condition. (Table 11.1) If the Y played no role in sex determination, what role did the X chromosomes play? Bridges suggested that there was a balance between the X chromosomes and the autosomes.4 In the diploid female the ratio was 2X:2A = 1; in the diploid male it was 1X:2A = 0.5. In the triploid, the The Balance Theory of Sex Determination 73 balance was 3X:3A =1, which made her a fertile female. But 2X:3A = 0.67 was intermediate between male and female, which accounted for the intersex appearance of those flies. Similarly, 1X:3A = 0.33 was an imbalanced or sterile male, and 3X:2A =1.50 was an imbalanced sterile female. BridgesclaimedthatiftherewasaviablehaploidwithanXchromosome, it would be 1X:1A = 1.0, which would make it a fertile female. Note that Bridges’s prediction for the fruit fly is the opposite of the situation for haplodiploidy, where a haploid Hymenopteran is a male. Balance theory also...