A programmed Mendelian violation maintains heterozygosity in a parthenogenetic ant

Parthenogenesis arises sporadically across the animal phylogeny, evolving via mutations that perturb sex and meiosis. The underlying mechanisms are rarely understood, but might provide insights into fundamental meiotic processes and the evolution of asexuality. Here, we investigate parthenogenesis in the clonal raider ant, Ooceraea biroi, which produces diploid offspring via the fusion of two haploid products from a single meiosis. Similar to inbreeding, this process should cause rapid genotypic degeneration due to loss of heterozygosity, which should result if crossover recombination is followed by random (Mendelian) segregation of chromosomes. However, by comparing whole genomes of mothers and daughters, we show that loss of heterozygosity is exceedingly rare, raising the possibility that crossovers are rare or absent from 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 co-segregate rather than segregate randomly. This discovery highlights an extreme example of cellular “memory” of crossovers, which could be a common yet cryptic feature of chromosomal segregation.