Mutations perturbing petal cell shape and anthocyanin synthesis influence bumblebee perception of Antirrhinum majus flower colour

Abstract

We wished to understand the effects on pollinator behaviour of single mutations in plant genes controlling flower appearance. To this end, we analysed snapdragon flowers (Antirrhinum majus), including the mixta and nivea mutants, in controlled laboratory conditions using psychophysical tests with bumblebees. The MIXTA locus controls petal epidermal cell shape, and thus the path that incident light takes within the pigment-containing cells. The effect is that mixta mutant flowers are pink in comparison to the wild type purple flowers, and mutants lack the sparkling sheen of wild type flowers that is clearly visible to human observers. Despite their fundamentally different appearance to humans, and even though bees could discriminate the flowers, inexperienced bees exhibited no preference for either type, and the flowers did not differ in their detectability in a Y-maze—either when the flowers appeared in front of a homogeneous or a dappled background. Equally counterintuitive effects were found for the non-pigmented, UV reflecting nivea mutant: even though the overall reflectance intensity and UV signal of nivea flowers is several times that of wild type flowers, their detectability was significantly reduced relative to wild type flowers. In addition, naïve foragers preferred wild type flowers over nivea mutants, even though these generated a stronger signal in all receptor types. Our results show that single mutations affecting flower signal can have profound effects on pollinator behaviour—but not in ways predictable by crude assessments via human perception, nor simple quantification of UV signals. However, current models of bee visual perception predict the observed effects very well.