A key floral scent component (β‐trans‐bergamotene) drives pollinator preferences independently of pollen rewards in seep monkeyflower

Floral odours play an important role in attracting insect pollinators. Because pollinators visit flowers to obtain pollen and nectar rewards, they should prefer floral odour profiles associated with the highest‐rewarding flowers (honest signals). In previous work, bumblebees exhibited a preference for flowers from outbred over inbred Mimulus guttatus plants. Pollen is the only floral reward in M. guttatus, and pollen viability (a reliable indicator of protein content) is reduced in inbred plants. Yet, differences in pollen viability did not explain the observed preferences. In this study, we examined the floral volatile profiles of inbred and outbred M. guttatus to identify inbreeding effects and associations between volatile compounds and the number of viable pollen grains per flower, designated “PRQ” (pollen reward quality). We also conducted pairwise choice tests with Bombus impatiens to evaluate the ability of bees to discriminate between odours of rewarding and non‐rewarding flowers and to determine whether bumblebee preferences are explained by differences in the floral odours of inbred and outbred plants. Inbred plants exhibited reduced emission of β‐trans‐bergamotene, the second‐most abundant compound in the volatile blend of outbred plants. Furthermore, pollen and fertile anthers emitted nonadecane. Six other compounds in the floral blend were positively correlated with PRQ. There was no overlap between compounds affected by inbreeding and compounds associated with PRQ. Even when given prior experience foraging on M. guttatus, bumblebees did not distinguish between the floral odours of rewarding and non‐rewarding outbred plants. However, they preferred floral odours from non‐rewarding outbred plants over rewarding inbred plants. Bumblebees without prior experience of flowers preferred volatile blends with higher versus lower amounts of β‐trans‐bergamotene. Taken together, these results suggest that the volatile emissions of M. guttatus provide reliable indicators of pollen rewards (potential honest signals), but that the preference of bumblebees for outbred plants is not driven by these cues but rather by a sensory bias for β‐trans‐bergamotene. This may represent a subtle form of deceit‐pollination that allows plants to attract pollinators while minimizing investment in costly rewards. A plain language summary is available for this article. Plain Language Summary