Fruit scent chemistry: adaptation to seed dispersal interactions
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Fleshy fruits have evolved diverse traits to attract seed dispersers in response to frugivore behavior and sensory capacities. Fruit scent has been suggested to signal ripeness and nutritional quality, yet the volatile components involved and the information they convey remain poorly understood. It is unknown which information is encoded in fruit scent, whether plants actively synthesize these signals, and thus whether scent constitutes an evolved communication system shaping seed-dispersal interactions. Aliphatic esters, chemicals whose odor is often described as “fruity,” are abundant in some ripe fruits, especially those dispersed by animals which tend to rely on their sense of smell for fruit selection. Moreover, they have been argued to be associated with sugar content, potentially rendering them an honest signal and hence a hotspot of animal-plant chemical communication. We investigated whether aliphatic esters indicate fruit quality honestly and represent an adaptive trait shaped by disperser identity. Using 13 fig species ( Ficus spp.; Moraceae) in Madagascar, we quantified seed dispersal by multiple animals using a quantitative ecological network. We then quantified chemical signals and nutritional rewards using thermal desorption gas chromatography-mass spectrometry (TD-GCMS) and high-performance liquid chromatography (HPLC), and used genome-guided transcriptome assembly to identify the candidate genes responsible for ester signaling. Our results show that (a) aliphatic esters occur more frequently in species dispersed primarily by olfactory-oriented mammals than in those dispersed by visually oriented birds; (b) ester abundance correlates positively with soluble sugar across species only in mammal-dispersed species, indicating an honest signal that is activated only when ecologically relevant; and (c) putative AAT gene revealing elevated expression associated with the increased abundance of aliphatic esters, sugars in single mammal-dispersed taxon. Together, these findings support the hypothesis that fruits have evolved to utilize the biochemical link between esters (signals) and sugars (rewards) to provide honest signals to seed dispersers.
Significance Statement
Fruit–frugivore communication is a critical component of ecological systems as it allows animals to find and identify ripe fruit, thus facilitating seed dispersal, plant reproduction, forest regeneration, and animal community maintenance. Chemical communication via fruit scent remains underexplored, particularly regarding the information encoded, active signal synthesis, and adaptive significance. Using a model system of wild figs from Madagascar, our study suggests that fruits have evolved to utilize aliphatic esters, a group of chemicals commonly described as “fruity” by human observers, to signal sugar levels to seed-dispersing animals. In species that rely on lemurs, which tend to rely strongly on their sense of smell, ester levels were higher than in bird-dispersed species, where visual signals are more prominent. Further, in lemur-dispersed species ester levels were correlated with sugar, indicating that they are reliably signaling fruit quality. Linking these patterns to elevated expression of the gene mediating ester biosynthesis, we also identify a molecular mechanism potentially under selection. These findings establish fruit scent as an adaptive communication system and reveal how plant chemicals evolve under mammalian selection.
