A role of territory formation in disruption of heterologous pairings in Drosophila male meiosis

Pairings between heterologous chromosomes in meiosis can lead to nondisjunction and the production of aneuploid gametes. To minimize these aberrant outcomes, organisms have evolved mechanisms to disrupt such improper pairings prior to orientation and segregation. In the male fruit fly, Drosophila melanogaster, bivalents segregate to distinct nuclear domains in prophase I, and it has been proposed that the formation of these distinct territories may play a role in disrupting interactions between limited homologies on heterologous chromosomes. To test this, we used fluorescent in situ hybridization to examine pairing between the X chromosome and Dp(1;3) chromosomes in which a segment of the X had been transposed to chromosome 3. We found that 120kb of homology was sufficient to insure nearly complete pairing but was not sufficient to direct merotelic segregation of the paired elements, suggesting that such pairings were being disrupted. We compared the perdurance of X / Dp(1;3) pairings to that of X / Dp(1;Y) pairings (in which homologs are paired),and found that heterologous pairings were disrupted at a higher frequency at the S2b stage of prophase I, the stage at which territory formation is initiated. Our results support the model that movement of bivalents into distinct domains in prophase I provides a mechanism to disrupt pairings between limited regions of homology, and thus may be one means of preventing improper segregation of heterologs in this organism.