To bee or not to bee: The ‘raison d'être’ of toxic secondary compounds in the pollen of Boraginaceae

While the presence of secondary compounds in floral nectar has received considerable attention, much less is known about the ecological significance and evolutionary origin of secondary ‘toxic’ compounds in pollen. It is unclear whether the presence of these compounds in pollen is non-adaptive and due to physiological ‘spillover’ from other floral tissues, or whether these compounds serve an adaptive function related to plant–pollinator interactions, such as protection of pollen against pollen thieves. Combining an experimental approach with phylogenetic comparative methods, and using western Palaearctic Boraginaceae as a model system, we investigate how pollen secondary metabolites influence, and are influenced by, relationships with bees, the main functional group of pollen-foraging pollinators. We found a significant relationship between the levels of secondary compounds in the corollas and those in the pollen in the investigated species of Boraginaceae, suggesting that baseline levels of pollen secondary compounds may partly be due to spillover from floral tissues. At realistic levels, pollen secondary compounds showed significant detrimental effects on bee pre-imaginal development, in agreement with previous egg-transfer experiments showing that in some cases Boraginaceae pollen did not support pre-imaginal development in bees not specialized on these plants. We also show that phylogenetically independent Boraginaceae taxa rewarding pollinators with pollen in addition to nectar exhibit significantly lower levels of toxic compounds in the pollen than taxa where the main reward is postulated to be nectar. Lastly, in contrast to our predictions, there was no positive association between toxin levels in the pollen of a given plant taxon and the number of bee species specialized on this taxon. We integrate all these findings and formulate an evolutionary scenario to account for the presence of toxic compounds in the pollen of Boraginaceae. We suggest that baseline levels of toxic compounds may be found in pollen due to spillover from other floral tissues and not primarily because of bee–flower interactions. Since pollen toxins can have detrimental effects on bees, we propose that selection acts to lower pollen toxin levels in plants where pollen, in addition to nectar, serves as a reward to bees. A free Plain Language Summary can be found within the Supporting Information of this article.