Do divergent mitochondrial backgrounds alter the fate of nuclear alleles during hybridization and admixture?

Abstract

Hybridization brings together genetic variation from different populations or species into admixed genomes. As selection sorts this variation, the fate of each allele is determined by its fitness effect in the new hybrid genomic background. Because mitochondrial genes coevolve with the nuclear genome, they may be especially sensitive to foreign nuclear backgrounds, making them potential "hot-spots" for hybrid incompatibilities. Here, we test whether selection against mitonuclear incompatibilities drives repeatable hybridization outcomes. Specifically, we experimentally evolved three sets of five populations of hybrid Drosophila melanogaster, each carrying the same nuclear chromosomes but paired with one of three increasingly divergent mitochondrial DNA backgrounds. We hypothesized that accumulated incompatibilities would result in different patterns of nuclear admixture among mitochondrial backgrounds. To test this, we tracked nuclear allele frequencies in all 15 populations by whole-genome sequencing at intermediate time points. After 25 generations, we observed that rapid genomic evolution produced a strikingly parallel mosaic of both nuclear ancestries, independent of mitochondrial background. Contrary to our hypothesis, we found no evidence that mitochondrial background1 shaped nuclear admixture, even for interspecific combinations. These results suggest that in species with large effective population sizes, efficient purifying selection limits the accumulation of mitonuclear incompatibilities, allowing selection on nuclear alleles to promote repeatable ancestry sorting immediately following hybridization.