Inseparability of X-Heterochromatic Functions Responsible for X:Y Pairing, Meiotic Drive, and Male Fertility in Drosophila melanogaster

Deficiencies encompassing part or all of the X heterochromatin of Drosophila melanogaster have been linked to three abnormalities in male meiosis and spermatogenesis: X-Y nondisjunction, skewed sperm recovery ratios favoring sperm with reduced chromatin content, and sterility in males carrying either a Y-autosome translocation or mal ⁺Y. In this study, 18 X heterochromatic deficiencies of varying sizes were tested in XY males for their spermatogenic phenotypes. All 18 proved to be either mutant for all three phenotypes or wild type for all three. Although variable among mutant deficiencies, expression levels of all three phenotypes were strongly correlated. Deficiencies that cause high levels of nondisjunction also cause severe recovery ratio distortion and are completely sterile in conjunction with mal⁺ Y. Low nondisjunction deficiencies cause comparable mild effects for the other phenotypes. The same deficiencies were also tested in males carrying a large heterochromatic free X duplication Dp(1; f)3. For all deficiencies which induce nondisjunction in XY males, the Y and free duplication pair regularly and the X fails to pair in XYDp males. Drive levels are constant across deficiencies in these males. Thus elimination of variability in the pairing phenotype also eliminates variability in sperm recovery ratios.