Repeated evolution of a reproductive polyphenism in plants is strongly associated with bilateral flower symmetry

Polyphenisms are a special type of phenotypic plasticity in which the products of development are not continuous but instead are separate and distinct phenotypes produced in the same genetic background. One of the most widespread polyphenisms in the flowering plants is cleistogamy, in which the same individual plant produces both open, cross-pollinated flowers as well as highly reduced and closed, self-pollinated (cleistogamous) flowers.^1-5 Cleistogamy is not a rare evolutionary phenomenon. It has evolved independently at least 41 times.¹ But what favors the evolution of cleistogamy is still largely unknown.¹ Darwin⁶ proposed a hypothesis that has never been properly tested. He observed that cleistogamy is more common in taxa with bilaterally symmetric (zygomorphic) flowers than in those with radially symmetric (actinomorphic) flowers. Moreover, Darwin suggested that cleistogamous flowers help to ensure pollination, which he postulated is less certain in zygomorphic taxa that rely on more specialized groups of pollinators. Here, we combined the largest datasets on floral symmetry and cleistogamy and used phylogenetic approaches to show that cleistogamy is indeed disproportionately associated with zygomorphic flowers and that zygomorphic species are more likely to evolve cleistogamy than actinomorphic species. We also show that zygomorphic species are less capable of autonomous open-flower self-pollination (lower autofertility), suggesting that selection of cleistogamy via reproductive assurance in zygomorphic taxa could help account for Darwin's observation. Our results provide support for the hypothesis that polyphenisms are favored when organisms encounter contrasting environments.