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Influence of sex-organ positions on pollen transfer and self-interference in plants with stylar polymorphisms: An experimental approach using three-dimensional printed flowers

Ferrero, Victoria1; Navarro, Luis2; Thomson, James3; Barrett, Spencer3

Published Jun 27, 2025 on Dryad. https://doi.org/10.5061/dryad.ffbg79d6q

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Jun 27, 2025 version files 20.46 KB

Abstract

Heterostylous plants are characterized by the reciprocal placement of stigmas and anthers in the floral morphs. Darwin proposed that this arrangement increases the proficiency of disassortative (intermorph) pollen transfer. The floral polymorphism may also function to avoid gamete wastage by reducing interference between sex organs. Distylous populations consist of two morphs: the long-styled morph with stigmas above anthers and the short-styled morph with stigmas below anthers. A related floral polymorphism – stigma-height dimorphism – involves floral morphs that differ in stigma-height but not anther position.

We used three-dimensional printed artificial flowers, with attached styles and anthers from glasshouse-grown Petunia grandiflora, to investigate whether sex-organ positioning simulating distyly and two forms of stigma-height dimorphism influence patterns of pollen transfer. Artificial flowers were arranged in flight cages and pollen transfer within and among flowers was mediated by captive bumble bees (Bombus impatiens) from commercial colonies. At the end of each trial, we quantified pollen grain number on stigmas and styles and the amount remaining in anthers of pollen donors. 

We found partial support for Darwin’s hypothesis on the probability of pollen reaching stigmas of the opposite morph, especially in the S-morph of distylous arrays. The number of pollen grains deposited on stigmas was influenced by the amount of time bumble bees spent foraging on flowers, which was significantly longer in the long-styled morph resulting in higher pollen loads in comparison with the short-styled morph. Self-interference in the form of self-pollen deposition on stigmas of donor flowers depended on the spatial separation of sexual organs. As predicted, we found higher self-pollen deposition in stigma-height dimorphic than distylous arrays. 

Although our results do not provide unequivocal support for Darwin’s pollen-transfer hypothesis, they confirmed that the morphological arrangement of sexual organs within flowers influenced pollen transfer patterns and levels of self-interference. They also indicated that variation in sex-organ deployment affects bumble bee foraging times with consequences for amounts of pollen deposited on stigmas. Although preliminary, our results highlight that three-dimensional printed flowers provide future opportunities to investigate the functional significance of variation in floral design in the context of plant-pollinator interactions.