Shared selection and genetic architecture drive strikingly repeatable evolution in long-term experimental hybrid populations

Abstract

The degree to which evolution repeats itself has implications regarding the major forces driving evolution and the potential for evolutionary biology to be a predictive (versus solely historical) science. To understand the factors that control evolutionary repeatability, we experimentally evolved four replicate hybrid populations of sunflowers at natural sites for up to 14 years and tracked ancestry across the genome. We found that there was very strong negative selection against introgressed ancestry in several chromosomes, but positive selection for introgressed ancestry in one chromosome. Further, the strength of selection was influenced by recombination rate. High recombination regions had lower selection against introgressed ancestry due to more frequent recombination away from incompatible backgrounds. Strikingly, evolution was highly parallel across replicates, with shared selection driving 88% of variance in introgressed allele frequency change. Parallel evolution was driven by both high levels of sustained linkage in introgressed alleles and strong selection on large-effect quantitative trait loci. This work highlights the repeatability of evolution through hybridization and confirms the central roles that natural selection, genomic architecture, and recombination play in the process.