To bee or not to bee – the “raison d’être” of toxic secondary compounds in the pollen of Boraginaceae

Authors: TRUNZ, VINCENT - Neuchatel University - Switzerland; LUCCHETTI, MATTEO - Neuchatel University - Switzerland; BENON, DIMITRI - Neuchatel University - Switzerland; DORCHIN, ACHIK - Tel Aviv University; DESURMONT, GAYLORD - European Biological Control Laboratory (EBCL); KAST, CHRISTINA - Agroscope; RASMANN, SERGIO - Neuchatel University - Switzerland; GLAUSER, GAETAN - Neuchatel University - Switzerland; PRAZ, CHRISTOPHE - Neuchatel University - Switzerland

Submitted to: Functional Ecology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 4/11/2020
Publication Date: 5/1/2020
Citation: Trunz, V., Lucchetti, M., Benon, D., Dorchin, A., Desurmont, G., Kast, C., Rasmann, S., Glauser, G., Praz, C. 2020. To bee or not to bee – the “raison d’être” of toxic secondary compounds in the pollen of Boraginaceae. Functional Ecology. 34(7):1345-1357. https://doi.org/10.1111/1365-2435.13581.
DOI: https://doi.org/10.1111/1365-2435.13581

Interpretive Summary: Pollen and nectar are rewards that flowering plants provide to pollinators in exchange to the dispersal of their pollen. However, the pollen of certain flowers is known to contain toxins that may harm pollinators. What is the origin and evolutionary significance of pollen toxins? Here we combined experiments where bee larvae were provided with pollen containing toxins and toxin-free pollen, and a comparative study of the amount of toxins present in the pollens of many species of one plant family (Boraginaceae) and an examination of their associated pollinators. The results of the study showed that the natural levels of toxins present in certain flowers can harm bee larvae and impede their development. In the Boraginaceae family, the amounts of toxins present in the pollens and in other floral tissues were positively correlated. This suggests that toxins may be present in pollen as a "spill-over" effect from other plant tissues where they act as anti-herbivore defenses. Plants that provide only pollen as a reward to pollinators tended to have lower amounts of toxins in their pollens than plants providing both pollen and nectar as rewards. This suggests that natural selection reduces the toxicity of pollen over evolutionary time for flowers that solely provide pollen to their pollinators.

Technical Abstract: 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 due to physiological “spill-over” from other floral tissues, or whether these compounds serve an adaptive function related to plant-pollinator interactions. Combining an experimental approach with phylogenetic comparative methods, and using western Palearctic 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 the evolutionary origin of pollen secondary compounds may be partly due to spill-over from floral tissues. At realistic levels, pollen secondary compounds showed significant detrimental effects on bee larval development, in agreement with previous egg-transfer experiments showing that in some cases Boraginaceae pollen did not support larval development in bees not specialized on these plants. We also show that Boraginaceae taxa where pollen acts as a reward in addition to nectar exhibit significantly lower levels of toxic compounds in the pollen than taxa where the main reward is nectar. Lastly, in contrast to our predictions, bees did not tend to specialize on plant taxa with high levels of secondary compounds in the pollen. 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 these compounds are primarily found in pollen due to spill-over from other floral tissues and not because of beeflower interactions. Since pollen toxins can have detrimental effects on bees by affecting their larvae, we propose that selection acts to lower pollen toxin levels in plants where pollen, in addition to nectar, serves as a reward to bees.