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.

Ex situ origins and dispersal of taxa have played important roles in the assembly of island-like biodiversity hotspots. Insular limestone karsts in Southeast Asia are hotspots of biodiversity and endemism, but the immigration processes of their unique floras are still poorly known. Here, we used Gesneriaceae as a proxy to investigate immigration dynamics of tropical and subtropical Southeast Asian karst floras. We show that immigration into subtropical Southeast Asian karst floras first occurred in the early Miocene, with two peaks in the early to middle Miocene and the Pliocene to early Pleistocene, whereas immigration into tropical Southeast Asian karsts initiated in the late Eocene, with two peaks in the late Oligocene and the late Miocene. The rich geological and ecological diversities of different regions, together with habitat isolation due to climatic changes, might be responsible for the different immigration patterns. We also discover that Southeast Asian karst biodiversity comprises a mix of immigrant pre-adapted lineages and descendants from local acid soil ancestors, although niche shift from acid soil to karst in tropical Southeast Asian islands was lacking. These findings provide insights into how Southeast Asian karsts respond to ongoing climate change and are of particular importance for their conservation planning.