Studies on nonhomologous chromosome pairing in females and a maternally suppressed position-effect lethal in males of Drosophila melanogaster

In the absence of structural heterozygosity in females of Drosophila melanogaster, the frequency of compound autosome nonsegregation is generally in the range of 0.5 to 5.0 percent. However, the frequency of nonsegregation for any given combination of compounds is highly reproducible. This low frequency of nonsegregation is commonly referred to as the spontaneous level of nonsegregation. By mating compound-3 females, with marked X-chromosomes, to differentially marked compound-3 males, it has been possible to demonstrate that nonsegregation of the compound autosomes is directly correlated with and proportional to nondisjunction of the X-chromosomes. In addition, the majority of female progeny that are patroclinous for the pair of compound autosomes are matroclinous for both X-chromosomes and, in most cases, the male progeny that are matroclinous for the pair of compound autosomes are patroclinous for the X-chromosome. From this distribution of X-chromosomes and compound autosomes it is evident that the simplest explanation for the recovery of exceptional progeny is nonhomologous pairing between the compound autosomes and the X-chromosomes. The presence of crossover X-chromosomes in a portion of nonsegregational exceptions indicates that not all nonsegregational progeny are derived following nonhomologous pairing of compound autosomes and X-chromosomes. Such independent nonsegregational progeny might represent the true "spontaneous" level of nonsegregation. In contrast to nonsegregation of compound autosomes, with rare exceptions X-chromosome nondisjunction is strictly a function of their nonhomologous pairing with compound autosomes. The inverse correlation between X-chromosome recombination and X-chromosome nondisjunction not only provides added support to the concept of nonhomologous pairing but also agrees with the temporal sequence of Grell's (1962) distributive pairing model. On the assumption that nondisjunction is a function of nonhomologous pairing, the observed distribution of nondisjunctional X-chromosomes, relative to the assortment of compound autosomes, is consistent with a trivalent pairing model that views nondisjunction as primarily a consequence of both X-chromosomes pairing with, and segregating from, a single compound autosome. However, the formation of bivalents involving nonhomologues is also a possible contributing factor. The evidence given here strongly favours the concept that nonhomologous distributive pairing occurs at the centromeric region, rather than along the total length, of the chromosomes. In a number of experiments, where the male parents carried the Muller-5 (M-5) X-c.hromosome, the number of patroclinous nondis junctional (M-5/0) males recovered was much lower than the number of matroclinous, nondisjunctional (X/X/Y) females. This reduced viability of M-5/0 males has been realized for several years and believed to reflect a position-effect suppression of the ribosomal-RNA genes. However, the results of these experiments reveal that M-5/0 lethality is conditional and dependent on the parental origin of the M-5 chromosome. When the origin of this chromosome is paternal, M-5/0 males display very low viability; when the M-5 chromosome is inherited maternally, the viability expressed by M-5/0 males is equal to that of M-5 males carrying a Y-chromosome. Moreover, M-5/0 lethality is partially suppressed by certain combinations of compound autosomes, both when carried by the female parents and when carried by the M-5/0 progeny themselves. The direct and maternal suppressive effects of these compound autosomes are assumed to be caused either by a specific suppressor gene present on these compound autosomes or by a nonspecific effect exerted by their centromeric heterochromatin. To explain M-5/0 lethality and the maternal effect associated with it, a speculative model, based on the inactivity of chromosomes in sperm and a possible cytoplasmic preconditioning in eggs of M-5 females, is proposed.Science, Faculty ofZoology, Department ofGraduat