Nonrandom segregation during meiosis: the unfairness of females

Abstract

Most geneticists assume that chromosome segregation during meiosis is Mendelian (i.e., each allele at each locus is represented equally in the gametes). The great majority of reports that discuss non-Mendelian transmission have focused on systems of gametic selection, such as the mouse t-haplotype and Segregation distorter in Drosophila, or on systems in which post-fertilization selection takes place. Because the segregation of chromosomes in such systems is Mendelian and unequal representation of alleles among offspring is achieved through gamete dysfunction or embryonic death, there is a common perception that true disturbances in the randomness of chromosome segregation are rare and of limited biological significance. In this review we summarize data on nonrandom segregation in a wide variety of genetic systems. Despite apparent differences between some systems, the basic requirements for nonrandom segregation can be deduced from their shared characteristics: i) asymmetrical meiotic division(s); ii) functional asymmetry of the meiotic spindle poles; and iii) functional heterozygosity at a locus that mediates attachment of a chromosome to the spindle. The frequency with which all three of these requirements are fulfilled in natural populations is unknown, but our analyses indicate that nonrandom segregation occurs with sufficient frequency during female meiosis, and in exceptional cases of male meiosis, that it has important biological, clinical, and evolutionary consequences.

Segregation distortion in chicken and the evolutionary consequences of female meiotic drive in birds

“…Although experimental evidence for spindle pole asymmetry has been presented from insects and plants (Pardo-Manuel de Villena and Sapienza, 2001b), so far, no such evidence, nor apparent physical differences in comparisons of oocyte spindle poles have been detected in birds (Rutkowska and Badyaev, 2008). However, non-random segregation of chromosome rearrangements in chicken do indicate that spindle pools may be asymmetric in birds as well (Dinkel et al, 1979).…”

“…However, numerous processes such as true meiotic drive, gametic selection, postzygotic viability selection and maternal-fetal incompatibilities have the potential to distort segregation ratios away from the Mendelian expectation. Most scientific attention has so far been directed towards post-meiotic processes, although the frequency and biological significance of true segregation distortion (SD) during meiosis remains poorly characterized (Pardo-Manuel de Villena and Sapienza, 2001b). In this study, we first discuss the potential for SD during avian meiosis, and then use two independent strategies to look for signs of SD in birds.…”

“…Pardo-Manuel de Villena and Sapienza (2001b) identified three conditions required for non-random segregation of chromosomes during meiosis. The first condition implies that the meiotic division needs to be asymmetric with regard to cell fate.…”

“…The first condition implies that the meiotic division needs to be asymmetric with regard to cell fate. In birds, as in many other eukaryotes, female meiosis proceeds through two rounds of asymmetrical cell divisions, each of which produce an oocyte and a polar body, in the end resulting in the production of only one functional gamete (Pardo-Manuel de Villena and Sapienza, 2001b;Rutkowska and Badyaev, 2008). This is in contrast to the symmetrical male meiosis, in which all four chromatids present before cell division will be represented in the final gametes.…”

“…This is in contrast to the symmetrical male meiosis, in which all four chromatids present before cell division will be represented in the final gametes. If chromosomes are partitioned non-randomly among oocyte and polar body, this asymmetry will lead to SD during female meiosis (Pardo-Manuel de Villena and Sapienza, 2001b).…”