Repeated Evolution of Storage Root and Invasions of Alpine Biome Drove Replicated Radiations of the Megadiverse Corydalis (Papaveraceae) in the Qinghai–Tibet Plateau

Abstract The interplay of key innovation and ecological opportunity is commonly recognized to be the catalyst for rapid radiation. Underground storage organs (USOs), as a vital ecological trait, are advantageous for adaptation of plants to extreme environments, but receive less attention compared to aboveground organs. Repeated evolution of various USOs has occurred across the plant tree of life. However, whether repeated occurrences of a USO in different clades of a group can promote its replicated radiations in combination with the invasion of similar environments remains poorly known. Corydalis is a megadiverse genus in Papaveraceae and exhibits remarkable variations in USO morphology and biome occupancy. Here, we first generated a robust phylogeny for Corydalis with wide taxonomic and genomic coverage based on plastome and nuclear ribosomal DNA sequence data. By dating the branching events, reconstructing ancestral ranges, evaluating diversification dynamics, and inferring evolutionary patterns of USOs and biomes and their correlations, we then tested whether the interplay of USO evolution and biome shifts has driven rapid diversification of some Corydalis lineages. Our results indicate that Corydalis began to diversify in the Qinghai–Tibet Plateau (QTP) at ca. 41 Ma, and 88% of dispersals happened through forests, suggesting that forests served as important dispersal corridors for range expansion of the genus. The storage root has originated independently at least six times in Corydalis since the Miocene, and its acquisition could have operated as a key innovation towards the adaptation to the alpine biome in the QTP. Repeated evolution of this game-changing trait and invasions of alpine biome, in combination with geoclimatic changes, could have jointly driven independent radiations of the two clades of Corydalis in the QTP at ca. 6 Ma. Our study provides new insights into the joint contribution of USO repeated evolution and biome shifts to replicated radiations, hence increasing our ability to predict evolutionary trajectories in plants facing similar environmental pressures. [Biome shift; diversification rates; Papaveraceae; phylogenomics; Qinghai–Tibet Plateau; underground storage organs.]