Angiosperms are the cornerstone of most terrestrial ecosystems and human livelihoods^1,2. A robust understanding of angiosperm evolution is required to explain their rise to ecological dominance. So far, the angiosperm tree of life has been determined primarily by means of analyses of the plastid genome^3,4. Many studies have drawn on this foundational work, such as classification and first insights into angiosperm diversification since their Mesozoic origins^5–7. However, the limited and biased sampling of both taxa and genomes undermines confidence in the tree and its implications. Here, we build the tree of life for almost 8,000 (about 60%) angiosperm genera using a standardized set of 353 nuclear genes⁸. This 15-fold increase in genus-level sampling relative to comparable nuclear studies⁹ provides a critical test of earlier results and brings notable change to key groups, especially in rosids, while substantiating many previously predicted relationships. Scaling this tree to time using 200 fossils, we discovered that early angiosperm evolution was characterized by high gene tree conflict and explosive diversification, giving rise to more than 80% of extant angiosperm orders. Steady diversification ensued through the remaining Mesozoic Era until rates resurged in the Cenozoic Era, concurrent with decreasing global temperatures and tightly linked with gene tree conflict. Taken together, our extensive sampling combined with advanced phylogenomic methods shows the deep history and full complexity in the evolution of a megadiverse clade.

C ₄ photosynthesis is a series of anatomical and biochemical modifications to the typical C ₃ pathway that increases the productivity of plants in warm, sunny, and dry conditions. Despite its complexity, it evolved more than 62 times independently in flowering plants. However, C ₄ origins are absent from most plant lineages and clustered in others, suggesting that some characteristics increase C ₄ evolvability in certain phylogenetic groups. The C ₄ trait has evolved 22–24 times in grasses, and all origins occurred within the PACMAD clade, whereas the similarly sized BEP clade contains only C ₃ taxa. Here, multiple foliar anatomy traits of 157 species from both BEP and PACMAD clades are quantified and analyzed in a phylogenetic framework. Statistical modeling indicates that C ₄ evolvability strongly increases when the proportion of vascular bundle sheath (BS) tissue is higher than 15%, which results from a combination of short distance between BS and large BS cells. A reduction in the distance between BS occurred before the split of the BEP and PACMAD clades, but a decrease in BS cell size later occurred in BEP taxa. Therefore, when environmental changes promoted C ₄ evolution, suitable anatomy was present only in members of the PACMAD clade, explaining the clustering of C ₄ origins in this lineage. These results show that key alterations of foliar anatomy occurring in a C ₃ context and preceding the emergence of the C ₄ syndrome by millions of years facilitated the repeated evolution of one of the most successful physiological innovations in angiosperm history.

Significance: Duplication of genomes following hybridization (allopolyploidy) is common among flowering plants, particularly in the grasses that cover vast areas of the world and provide food and fuel. Here, we find that genome duplication has occurred at a remarkable rate, accounting for at least a third of all speciation events in a group of about 1,200 species. Much of this genome duplication occurred during the expansion of the C₄grasslands in the Late Miocene. We find no evidence that allopolyploidy leads directly to a change in the net rate of diversification or correlates with the origin of novel morphological characters. However, as a mode of speciation, the frequency of allopolyploidization is surprisingly high.