Diverging Arabidopsis populations quickly accumulate pollen-acting genetic incompatibilities

The process by which species diverge from one another, gradually accumulate genetic incompatibilities, and eventually reach full-fledged reproductive isolation is a key question in evolutionary biology. However, the nature of reproductive barriers, the pace at which they accumulate, and their genomic distribution remain poorly documented. The disruption of co-adapted epistatic interactions in hybrids and the accumulation of selfish genetic elements are proposed contributors to this process, and can lead to the distortion of the Mendelian segregation of the affected loci across the genome. In this study we detect and quantify segregation distortion across the genomes of crosses produced from a diverse sampling of Arabidopsis lyrata and A. halleri populations, 2 species at the early stages of speciation and that can still interbreed. We observe no distortion loci in crosses with geographically and genetically similar parents, but both their frequency of occurrence and their magnitude become highly variable in more distant crosses. We also observe that distorter loci evolve rapidly, as they occur not only in interspecific hybrids, but also in intraspecific hybrids produced by crossing individuals from 2 isolated regions. Finally, we identify both genome-wide nonindependence and 2 specific genomic regions on different chromosomes where opposite distortion effects are repeatedly observed across multiple F1 individuals, suggesting negative epistasis is a major contributor to the evolution of hybrid segregation distortion. Our study demonstrates that pollen-acting segregation distortion is ubiquitous, and may contribute not only to the ongoing reproductive isolation between A. halleri and A. lyrata, but also between recently diverged populations of the same species.