Recurrent genome duplication events likely contributed to both the ancient and recent rise of ferns.

Abstract

Ferns, the second largest group of vascular plants, originated ~400 million years ago (Mya). They became dominant in the ancient Earth landscape before the angiosperms and are still important in current ecosystems. Many ferns have exceptionally high chromosome numbers, possibly resulting from whole-genome duplications (WGDs). However, WGDs have not been investigated molecularly across fern diversity. Here we detected and dated fern WGDs using a phylogenomic approach and by calculating synonymous substitution rates (Ks). We also investigated a possible correlation between proposed WGDs and shifts in species diversification rates. We identified 19 WGDs: three ancient events along the fern phylogenetic backbone that are shared by 66%-97% of extant ferns, with additional lineage-specific WGDs for eight orders, providing strong evidence for recurring genome duplications across fern evolutionary history. We also observed similar Ks peak values for more than half of these WGDs, with multiple WGDs occurring close to the Cretaceous (~145-66 Mya). Despite the repeated WGD events, the biodiversity of ferns declined during the Cretaceous, implying that other factors probably contributed to the floristic turnover from ferns to angiosperms. This study provides molecular evidence for recurring WGDs in ferns and offers important clues to the genomic evolutionary history of ferns.