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The Ancestral Flower of Angiosperms and Its Early Diversification

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The Ancestral Flower of Angiosperms and Its Early Diversification

Hervé Sauquet et al. Nat Commun.

Abstract

Recent advances in molecular phylogenetics and a series of important palaeobotanical discoveries have revolutionized our understanding of angiosperm diversification. Yet, the origin and early evolution of their most characteristic feature, the flower, remains poorly understood. In particular, the structure of the ancestral flower of all living angiosperms is still uncertain. Here we report model-based reconstructions for ancestral flowers at the deepest nodes in the phylogeny of angiosperms, using the largest data set of floral traits ever assembled. We reconstruct the ancestral angiosperm flower as bisexual and radially symmetric, with more than two whorls of three separate perianth organs each (undifferentiated tepals), more than two whorls of three separate stamens each, and more than five spirally arranged separate carpels. Although uncertainty remains for some of the characters, our reconstruction allows us to propose a new plausible scenario for the early diversification of flowers, leading to new testable hypotheses for future research on angiosperms.

Conflict of interest statement

The authors declare no competing financial interests.

Figures

Figure 1
Figure 1. Three-dimensional model of the ancestral flower reconstructed from our analyses.
Here we provide the states with highest mean posterior probability and their associated credibility intervals from the reversible-jump Bayesian analysis of the C series of trees, which takes into account all forms of uncertainty (parameters, tree, branch times, model). States marked with three asterisks (***) indicate high confidence and consistency across methods of reconstruction (for example, perianth present, undifferentiated and actinomorphic). Other states need to be interpreted with caution as their reconstruction was either associated with higher uncertainty (for example, perianth phyllotaxis, number of stamen whorls) or inconsistent across methods (for example, sex reconstructed as equivocal with parsimony). The colours, shapes and relative sizes of organs were not inferred from our analyses and were chosen here for artistic reasons. The exact number of organs could not be reconstructed precisely. Minimum numbers were chosen for this representation, but reconstructions with more floral organs are also compatible with our results (for further details, see Supplementary Discussion, section ‘Reconstructing the ancestral flower’). A rotating version of this model is provided as Supplementary Movie 1.
Figure 2
Figure 2. Maximum likelihood ancestral state reconstruction of functional sex of flowers in angiosperms.
Our results show that bisexual flowers are ancestral and that unisexual flowers evolved many times independently. The pie charts at the centre of the figure indicate the proportional likelihoods for reconstructed ancestral states at 15 key nodes (here we illustrate character 100_A on the maximum clade credibility tree from the C series; for complete results, see Supplementary Data 1 and Supplementary Data 14–23). The photographs illustrate the diversity of angiosperm flowers (photographs by H.S., Y.S., J.S. and M.v.B.).
Figure 3
Figure 3. Overview of confidence in ancestral state reconstructions across all traits (X axis), focal nodes (Y axis) and sets of trees (panels).
Confidence scores on a three-star scale were attributed for each trait-node combination based on the cross-comparison of MP, ML and rjMCMC results and the lower bound of the rjMCMC credibility intervals (see Supplementary Discussion for details). A more detailed version of this figure with row and column captions is provided in Supplementary Data 1. Light=low confidence; dark=high confidence.
Figure 4
Figure 4. Simplified scenario for the earliest phase of floral diversification as inferred from our analyses.
Each floral diagram summarizes the main features of our reconstructed ancestors for key nodes of the tree (for details, see Supplementary Discussion and Supplementary Figs 2–7). This figure only depicts the presumed first 40 million years of floral evolution, without exhaustively representing every new morphology that arose during that time. The absolute timescale provided here corresponds to divergence time estimated with a narrow constraint on the maximum age of angiosperms; relaxing this constraint to reflect alternative studies that yielded older age estimates for angiosperms resulted in nearly identical ancestral reconstructions (see Supplementary Discussion). Note that there is uncertainty associated with some of these reconstructions (especially for Angiospermae, Magnoliidae and Eudicotyledoneae). Therefore, the scenario illustrated here is one of several plausible alternatives and should be taken with caution. Floral diagram colour code: light green=undifferentiated tepals; green=sepals; yellow=petals; red=stamens; blue=carpels.
Figure 5
Figure 5. Maximum likelihood ancestral state reconstructions of four representative floral characters.
The pie charts at the centre of the figure indicate the proportional likelihoods for reconstructed ancestral states at 15 key nodes (here we optimized the characters on the maximum clade credibility tree from the C series; for complete results, see Supplementary Data 1 and Supplementary Data 14–23). Grey branches denote missing, inapplicable or polymorphic data. (a) Ovary position (character 102_B). (b) Fusion of perianth (character 204_A). (c) Symmetry of perianth (character 207_B). (d) Number of perianth whorls (character 231_A).

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