Phylogenomics and the rise of the angiosperms

Abstract

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.

Fig. 1. Time-calibrated phylogenetic tree for angiosperms based on 353 nuclear genes.

All 64 orders, all 416 families and 58% (7,923) of genera are represented. The young tree is illustrated here (maximum constraint at the root node of 154 Ma), with branch colours representing net diversification rates. Black dots at nodes indicate the phylogenetic placement of fossil calibrations based on the updated AngioCal fossil calibration dataset. Note that calibrated nodes can be older than the age of the corresponding fossils owing to the use of minimum age constraints. Arcs around the tree indicate the main clades of angiosperms as circumscribed in this paper. ANA grade refers to the three consecutively diverging orders Amborellales, Nymphaeales and Austrobaileyales. Plant portraits illustrating key orders were sourced from Curtis’s Botanical Magazine (Biodiversity Heritage Library). These portraits, by S. Edwards, W. H. Fitch, W. J. Hooker, J. McNab and M. Smith, were first published between 1804 and 1916 (for a key to illustrations see Supplementary Table 2). A high-resolution version of this figure can be downloaded from 10.5281/zenodo.10778206 (ref. ).

Fig. 2. Diversification dynamics across angiosperms.

The results illustrated are based on the young tree (maximum constraint at the root node of 154 Ma). a, Time-calibrated summary phylogenetic tree with LTT plots rendered as heatmaps for all orders with four or more sampled genera. The log-transformed increase in the number of lineages is depicted in 5 Myr intervals, omitting crown nodes, which disproportionately altered the visualization; crown node locations are indicated by vertical lines. The yellow to blue colour scale represents steep to shallow slopes. For each order, the numbers of sampled and total genera are provided. b, A global LTT heatmap for all angiosperms is shown at the bottom of the figure as a whole.

Fig. 3. Angiosperm-wide diversification and gene tree conflict through time.

The results illustrated are based on the young tree (maximum constraint at the root node of 154 Ma). See Extended Data Fig. 5 for results based on the old tree. a, Estimated net diversification rate through time (yellow, left y axis) and the level of gene tree conflict through time (blue, right y axis). Net diversification rates are estimated with a model that enables speciation rates to vary between time intervals; the line is the posterior mean and the yellow shaded area is the 95% highest posterior density. Gene tree conflict is calculated from the percentage of gene trees that do not share a congruent bipartition with each species tree branch, with the plotted value being the mean across all species tree branches that cross each 2.5 Myr time slice. b, Cumulative percentage of extant orders and families that have originated through time. In both a and b, the background grey-scale gradient is the estimated percentage of extant lineages represented in the species tree through time (sampling fraction).

Fig. 4. Summary of lineage-specific diversification rate shifts estimated by BAMM.

The results illustrated are based on the young tree (maximum constraint at the root node of 154 Ma). See Extended Data Fig. 6 for results based on the old tree. a, Diversification rate increases per LTT. The colour corresponds to the average magnitude of the rate increases during the time period. b, Equivalent to a but for rate decreases. c, Equivalent to a but focusing on the largest 25% of diversification rate increases. In a, b and c, the number of shifts is from the maximum a posteriori shift configuration with the prior for the number of shifts set to 10 and the background grey-scale gradient is the estimated percentage of extant lineages represented in the species tree through time (sampling fraction).

Extended Data Fig. 1. Tanglegram at ordinal level between this work (left) and the APG IV schematic tree (right).

Branches colours represent the clades according to the composition proposed in each work. Posterior probability is presented only for nodes without maximum support. Coloured circles in the left tree represent the posterior probability of each node as: maximum (absent), between 1 and 0.95 (green), between 0.95 and 0.75 (yellow), between 0.75 and 0.5 (red), below 0.5 (black).

Extended Data Fig. 2. Comparison of node age estimates in the eight time-calibrated phylogenetic trees.

Each point represents a node and corresponds to the percentage difference in age estimates for that node between the two trees that are compared in each plot.

Extended Data Fig. 3. Comparison of stem ages of families and orders inferred in this study and Ramírez-Barahona et al..

a and b, Stem age comparison between our young tree (maximum constraint at the root node of 154 Ma) and the dataset CC_complete of Ramírez-Barahona et al.. a, Ages in each study, coloured according to taxonomic rank and b, Age differences, calculated as age in this study minus age in Ramírez-Barahona et al. c and d, Stem ages comparison between our old tree (maximum constraint at the root node of 247 Ma) and the dataset UC_complete from Ramírez-Barahona et al. c, Ages in each study, coloured according to taxonomic rank and d, Age differences, calculated as age in this study minus age in Ramírez-Barahona et al..

Extended Data Fig. 4. Correlation between branch time duration and percentage of gene trees that do not share a congruent bipartition for the branch.

The results are based on the young tree (maximum constraint at the root node of 154 Ma). For each branch in the young tree, the percentage of gene trees that do not share a congruent bipartition with the species tree branch is plotted against the logarithm of the time duration for the branch.

Extended Data Fig. 5. Angiosperm-wide diversification and gene tree conflict through time.

This is equivalent to Fig. 3 but for the old tree (maximum constraint at the root node of 247 Ma). a, Estimated net diversification rate through time (yellow, left y-axis) and the level of gene tree conflict through time (blue, right y-axis). Net diversification rates are estimated with a model that enables speciation rates to vary between time intervals; the line is the posterior mean and the yellow shaded area is the 95% highest posterior density. Gene tree conflict is calculated from the percentage of gene trees that do not share a congruent bipartition with each species tree branch, with the plotted value being the mean across all species tree branches that cross each 2.5 Myr time slice. b, Cumulative percentage of extant orders and families that have originated through time. In both a and b, the background grey-scale gradient is the estimated percentage of extant lineages represented in the species tree through time (“sampling fraction”).

Extended Data Fig. 6. Summary of lineage-specific diversification rate shifts estimated by BAMM.

This is equivalent to Fig. 4, but for the old tree (maximum constraint at the root node of 247 Ma). a, Diversification rate increases per lineage through time. The colour corresponds to the average magnitude of the rate increases during the time period. b, Equivalent to a, but for rate decreases. c, Equivalent to a, but focusing on the largest 25% of diversification rate increases. In a, b and c, the number of shifts is extracted from the maximum a posteriori shift configuration, the prior for the number of shifts is set to 10 and the background grey-scale gradient is the estimated percentage of extant lineages represented in the species tree through time (“sampling fraction”).