Genetic evidence that nonhomologous disjunction and meiotic drive are properties of wild-type Drosophila melanogaster male meiosis

Abstract

We have followed sex and second chromosome disjunction, and the effects of these chromosomes on sperm function, in four genotypes: wild-type males, males deficient for the Y-linked crystal locus, males with an X chromosome heterochromatic deficiency that deletes all X-Y pairing sites, and males with both deficiencies. Both mutant situations provoke chromosome misbehavior, but the disjunctional defects are quite different. Deficiency of the X heterochromatin, consonant with the lack of pairing sites, mostly disrupts X-Y disjunction with a decidedly second-level effect on major autosome behavior. Deleting crystal, consonant with the cytological picture of postpairing chromatin-condensation problems, disrupts sex and autosome disjunction equally. Even when the mutant-induced nondisjunction has very different mechanics, however, and even more importantly, even in the wild type, there is strong, and similar, meiotic drive. The presence of meiotic drive when disjunction is disrupted by distinctly different mechanisms supports the notion that drive is a normal cellular response to meiotic problems rather than a direct effect of particular mutants. Most surprisingly, in both wild-type and crystal-deficient males the Y chromosome moves to the opposite pole from a pair of nondisjoined second chromosomes nearly 100% of the time. This nonhomologous interaction is, however, absent when the X heterochromatin is deleted. The nonhomologous disjunction of the sex and second chromosomes may be the genetic consequence of the chromosomal compartmentalization seen by deconvolution microscopy, and the absence of Y-2 disjunction when the X heterochromatin is deleted suggests that XY pairing itself, or a previously unrecognized heterochromatic function, is prerequisite to this macrostructural organization of the chromosomes.

Figure 1.

Origins and phenotypes of progeny produced in crosses to attached-2 females.

Figure 2.

Frequencies per parental male of second chromosome and sex chromosome nondisjunction. Second chromosome nondisjunction per male is calculated as (2 × progeny)/male for the crosses to C(2)EN females, and sex chromosome nondisjunction per male is calculated as (exceptional progeny)/male for the free-2 crosses (see text).

Figure 3.

Meiotic rate of sex chromosome nondisjunction in cells in which the second chromosomes have disjoined normally and in cells in which the second chromosomes have nondisjoined. Maximum-likelihood estimates were obtained numerically using the MLIKELY.PAS program. The 95% support intervals shown are the nondisjunction rates at which likelihood-ratio comparisons with the best estimates yield G > 3.842.

Figure 4.

Disjunctional interactions between the sex and second chromosomes. Maximum-likelihood estimates and support intervals for the rates of separation of the Y and second chromosomes to opposite poles (D₂) or of nondisjunctional sex chromosomes and the second chromosomes to opposite poles (D₃) were found as described in Figure 3.

Figure 5.

Chromosome-specific effects on sperm function. Maximum-likelihood estimates and support intervals for R_X, R_Y, and R₂ were found as indicated in Figure 3. Values of R_X and R_Y for the crosses to free-2 females are indicated by diamonds; the values for the wild-type × free-2 cross are particularly unreliable because that cross produced only four nondisjunctional offspring.