Self-medicating behavior in bumble bees has cascading consequences for pollination and plant reproduction

The sublethal effects of parasites can profoundly influence host traits and propagate to other trophic levels via indirect effects. To date, research on such trait-mediated indirect effects of parasites has focused on non-adaptive changes to host behavior, but adaptive sickness behaviors, such as self-medication, could also indirectly affect community composition and even the evolution of medicinal traits in lower trophic levels. Here, we used interactions among the parasite Crithidia bombi, the bumble bee host Bombus impatiens, and Monarda fistulosa, a bee-pollinated plant with multiple chemotypes (genetically determined chemical phenotypes), to experimentally test whether parasite infection influences pollinator foraging, pollination success, and female plant reproduction differentially for medicinal vs. non-medicinal chemotypes. Compounds from three Monarda chemotypes reduced Crithidia infection intensity in bees (thymol, carvacrol, and 1,8-cineole; hereafter medicinal chemotypes), while two others did not ((R)-(-)-linalool and geraniol; hereafter non-medicinal chemotypes), compared to control sucrose solutions. We found evidence for self-medication in tent foraging choice assays: infected bees preferred medicinal chemotypes while uninfected bees foraged indiscriminately, leading to differences in pollen receipt. Crithidia infection had weak but compounding chemotype-specific effects on seed production, germination rate, and offspring chemotype, such that pollination by infected bees resulted in a 57% increase in the proportion of medicinal plants in the F1 generation compared to pollination by uninfected bees. Self-medicating behavior can have differential effects on the reproduction of medicinal vs. non-medicinal plants, suggesting that pollinator parasites may act as agents of selection on the phytochemistry of floral rewards. SIGNIFICANCE STATEMENTParasite infection can alter host behavior in multiple ways, including by inducing self-medication. Self-medication has been documented in diverse animal taxa, yet we know very little about the broader ecological or evolutionary consequences of this response to infection. Here, we demonstrate that bumble bees infected with a common parasite show a preference for plant genotypes whose nectar contains antiparasitic compounds, and that this results in differential pollination and reproductive success for medicinal vs. non-medicinal individuals of a chemically polymorphic plant species. Our findings highlight self-medication as a previously understudied mechanism by which parasite infection could initiate cascading effects across trophic levels, and suggest that parasites may indirectly influence the evolution of plant traits via pollinator self-medication behaviors.