November 2024
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Polyploidy, or whole-genome duplication (WGD), both a strong evolutionary and ecological force and a potential pitfall, occurs extensively across the tree of life, particularly in angiosperms. While polyploid organisms are prevalent, ancient polyploidy (paleopolyploidy) is decisively rare. Numerous studies have revealed adaptive changes at the genomic, cellular, and physiological levels that confer evolutionary advantages to polyploids, but the factors contributing to their long-term success remain poorly understood. Here, we assembled a large angiosperm genome dataset encompassing 470 different angiosperm species. We reconstructed a highly concordant evolutionary timescale of angiosperms and conducted a large-scale study to identify and date WGDs across this set of species. We unveiled 132 independent ancient WGD events that do not seem randomly distributed in time, but clustered around periods of great environmental upheaval. We observed that a majority of paleopolyploidizations occurred between 50 and 75 mya, coinciding with the Paleocene-Eocene Thermal Maximum and the Cretaceous-Paleogene (K-Pg) boundary. A more recent wave of ancient WGDs can be observed between 25 and 40 mya, coinciding with periods of glaciation expansion, rapid shifts in sea surface temperatures, and a marked decrease in global mean surface temperature. Integrating different lines of evidence, we argue that polyploids have an increased chance of survival during times of great environmental turmoil.