Meiotic behavior of compound autosomes in females of Drosophila melanogaster: interchromosomal effects and the source of spontaneous nonsegregation.

In females of Drosophila melanogaster, compound autosomes enter the repulsion phase of meiosis uncommitted to a particular segregation pattern because their centromeres are not restricted to a bivalent pairing complex as a consequence of crossing over. Their distribution at anaphase, therefore, is determined by some meiotic property other than exchange pairing, a property that for many years has been associated with the concept of nonhomologous pairing. In the absence of heterologous rearrangements or a free Y chromosome, C(3L) and C(3R) are usually recovered in separate gametes, that is as products of meiotic segregation. Nevertheless, there is a regular, albeit infrequent, recovery of reciprocal meiotic products (the nonsegregational products) that are disomic and nullosomic for compound thirds. The frequency of these exceptions, which is normally between 0.5 and 5.0%, differs for the various strains examined, but remains constant for any given strain. Since previous studies have not uncovered a cause for this base level of nonsegregation, it has been referred to as the spontaneous frequency. In this study, crosses between males and females whose X chromosomes, as well as compound autosomes, are differentially marked reveal a highly significant positive correlation between the frequency of compound-autosome nonsegregation and the frequency of X-chromosome nondisjunction. However, an inverse correlation is found when the frequency of nondisjunction is related to the frequency of crossing over in the proximal region of the X-chromosome. These findings have been examined with reference to the distributive pairing and the chromocentral models and interpreted as demonstrating (1) that nonsegregational meiotic events arise primarily as a result of nonhomologous interactions, (2) that forces responsible for the segregation of nonhomologous chromosomes are properties of the chromocentral region, and (3) that these forces come into expression after the exchange processes are complete.