Unselfish meiotic drive maintains heterozygosity in a parthenogenetic ant

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Abstract

According to Mendel’s second law, chromosomes segregate randomly in meiosis. Non-random segregation is primarily known for cases of selfish meiotic drive in females, in which particular alleles bias their own transmission into the oocyte 1,2 . Here, we report a rare example of unselfish meiotic drive for crossover inheritance in the clonal raider ant, Ooceraea biroi . This species produces diploid offspring parthenogenetically via fusion of two haploid nuclei from the same meiosis 3 . This process should cause rapid genotypic degeneration due to loss of heterozygosity, which results if crossover recombination is followed by random (Mendelian) segregation of chromosomes 4,5 . However, by comparing whole genomes of mothers and daughters, we show that loss of heterozygosity is exceedingly rare, raising the possibility that crossovers are infrequent or absent in O. biroi meiosis. Using a combination of cytology and whole genome sequencing, we show that crossover recombination is, in fact, common, but that loss of heterozygosity is avoided because crossover products are faithfully co-inherited. This results from a programmed violation of Mendel’s law of segregation, such that crossover products segregate together rather than randomly. This discovery highlights an extreme example of cellular “memory” of crossovers, which could be a common yet cryptic feature of chromosomal segregation.

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