Polyploid Origins and the Genomics of Adaptation in the Worldwide Weed Capsella bursa-pastoris

Whole genome duplication events have occurred repeatedly during flowering plant evolution, and there is growing evidence for predictable patterns of gene retention and loss following polyploidization. Despite these important insights, the rate and processes governing the earliest stages of diploidization remain uncertain, and the relative importance of genetic drift vs. natural selection in the process of gene degeneration and loss is unclear. Furthermore, many of the most successful worldwide weeds are polyploid, potentially due to a burst of positive selection following relaxation of pleiotropic constraints following whole genome duplication. Here we conduct whole genome resequencing in Capsella bursa-pastoris, a recently formed tetraploid with one of the most widespread species distributions of any angiosperm. Whole genome data provide strong support for recent hybrid origins of the tetraploid species within the last 100-300,000 years from two diploid progenitors in the Capsella genus. Major-effect inactivating mutations are frequent, but many were inherited from the parental species and show no evidence of being fixed by positive selection. Despite a lack of large-scale gene loss, we observe a shift in the efficacy of natural selection genome-wide. Our results suggest that the earliest stages of diploidization are associated with quantitative genome-wide shifts in the strength and efficacy of selection rather than rapid gene loss, and that nonfunctionalization can receive a 'head start' through deleterious variants found in parental diploid populations. Finally, we identify an enrichment of signals of positive selection on the subgenome originating from the outcrossing diploid progenitor compared with the selfing progenitor, suggesting that ancestral selective history plays an important role in ongoing adaptation in allopolyploid genomes.