Scent matters: differential contribution of scent to insect response in flowers with insect vs. wind pollination traits.

Abstract

Growing experimental evidence that floral scent is a key contributor to pollinator attraction supports its investigation as a component of the suite of floral traits that result from pollinator-mediated selection. Yet, the fate of floral scent during the transition out of biotic into abiotic pollination has rarely been tested. In the case of wind pollination, this is due not only to its rarer incidence among flowering plants compared with insect pollination, but also to the scarcity of systems amenable to genus-level comparisons. Thalictrum (Ranunculaceae), with its multiple transitions from insect to wind pollination, offers a unique opportunity to test interspecific changes in floral fragrance and their potential impact on pollinator attraction. First, the Thalictrum phylogeny was revised and the ancestral character state of pollination mode was reconstructed. Then, volatile organic compounds (VOCs) that comprise the scent bouquets of flowers from 11 phylogenetically representative wind- and insect-pollinated species were characterized and compared. Finally, to test the hypothesis that scent from insect-pollinated flowers elicits a significantly greater response from potential pollinators than that from wind-pollinated flowers, electroantennograms (EAGs) were performed on Bombus impatiens using whole flower extracts. Phylogenetic reconstruction of the pollination mode recovered 8-10 transitions to wind pollination from an ancestral insect pollination state and two reversals to insect pollination. Biochemical and multivariate analysis showed that compounds are distinct by species and only partially segregate with pollination mode, with no significant phylogenetic signal on scent composition. Floral VOCs from insect-pollinated Thalictrum elicited a larger antennal response from potential insect pollinators than those from wind-pollinated congeners. An evolutionary scenario is proposed where an ancestral ability of floral fragrance to elicit an insect response through the presence of specific compounds was independently lost during the multiple evolutionary transitions to wind pollination in Thalictrum.