Patterns of Population Variation in Two Paleopolyploid Eudicot Lineages Suggest That Dosage-Based Selection on Homeologs Is Long-Lived

Abstract

Genes that are inherently subject to strong selective constraints tend to be overretained in duplicate after polyploidy. They also continue to experience similar, but somewhat relaxed, constraints after that polyploidy event. We sought to assess for how long the influence of polyploidy is felt on these genes' selective pressures. We analyzed two nested polyploidy events in Brassicaceae: theAt-a genome duplication that is the most recent polyploidy in themodel plant Arabidopsis thaliana and a more recent hexaploidy shared by thegenus Brassica andits relatives. By comparing the strengthanddirectionof thenatural selectionactingat the population andat the species level, we find evidence for continued intensified purifying selection acting on retained duplicates from both polyploidies even down to the present. The constraint observed in preferentially retained genes is not a result of the polyploidy event: the orthologs of such genes experience even stronger constraint in nonpolyploid outgroup genomes. In both the Arabidopsis and Brassica lineages, we further find evidence for segregating mildly deleterious variants, confirming that the population-level data uncover patterns not visiblewith between-species comparisons. Using theA. thalianametabolic network, we also exploredwhether network position was correlated with the measured selective constraint. At both the population and species level, nodes/genes tended to show similar constraints to their neighbors. Our results paint a picture of the long-lived effects of polyploidy on plant genomes, suggesting that even yesterday's polyploids still have distinct evolutionary trajectories.