Whole genome sequencing of Dictyostelium discoideum meiotic progeny (and their parents) reveals frequent lateral transmission of mitochondrial DNA. Triparental inheritance in Dictyostelium

Sex promotes the recombination and reassortment of genetic material and is prevalent across eukaryotes. Although sex follows a conserved pattern in many well-studied organisms, details of sexual inheritance are scant in several major lineages. We report here the first genomewide characterisation of meiotic progeny in the social amoeba Dictyostelium discoideum. Sex in social amoebae has a number of unusual features: there is no block to multiple fertilization; zygotes feeds cannibalistically on conspecific cells; and meiosis occurs without Spo11, the enzyme that otherwise universally initiates meiotic recombination. We find that recombination occurs genomewide at high frequency in pairwise crosses between all three D. discoideum mating types. In crosses involving three strains, fusion of more than two gametes frequently leads to triparental inheritance, with recombined nuclear haplotypes inherited from two parents and the mitochondrial genome from a third. Cells that do not contribute genetically to the zygote nucleus thereby have a stake in the next haploid generation, so sexual selection acting on mitochondrial genomes may have a role in enforcing cooperation in this conflictual system. We demonstrate how this lateral transfer enables mitochondria to escape association with uncompetitive nuclei. This system provides fresh opportunities to investigate mitonuclear interactions and defences against cytoplasmic parasites, and we suggest that promiscuous cell fusions similar to those observed in Dictyostelium promoted the spread of mitochondria in proto-eukaryotes.