Linh M. N. Nguyen

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.

Plant–frugivore mutualisms are shaped by suites of fruit traits that evolve in tandem with the preferences of seed dispersers, a concept encapsulated by the dispersal syndrome hypothesis. While morphological characteristics (e.g., size, color, firmness) have been extensively studied, the nutritional dimension, and particularly sugar profiles, remains comparatively understudied. This is despite its role as a primary reward influencing frugivore foraging decisions and despite the fact that these are the primary attractants driving animal feeding and ultimately seed dispersal. Here, we investigated the evolutionary and ecological drivers of sugar profile diversity in the ripe fruits of 15 animal-dispersed wild fig (Ficus) species. We sampled 1019 ripe fruit samples of 50 individual trees at 4 different field sites in Madagascar. Fruits were oven-dried and analyzed using High‑Performance Liquid Chromatography to quantify the abundances of sugars. We addressed three questions: (Q1) Are sugar-composition profiles species-specific? (Q2) Is the sugar profile phylogenetically conserved? (Q3) Do sugar profiles covary with other fruit traits in ways that support dispersal syndromes? Our results demonstrate fig species exhibit certain distinct sugar profiles, alongside substantial intraspecific variability; we did not find a phylogenetic signal in sugar profiles, suggesting that sugar profiles are not strongly constrained by shared ancestry but have likely diverged under ecological selection; and sugar profiles covary significantly with other fruit traits. Species with smaller fruits, different/multiple coloration, and mixed aromatic profiles rich in terpene and ester exhibited elevated sucrose concentrations, whereas larger, more conspicuous, and ester-rich fruits tended to contain higher fructose levels. Together, these findings lend support for the dispersal syndrome hypothesis by demonstrating that sugar profile, like other non-sugar traits, such as morphology, has evolved in association with frugivore preferences.

Fleshy fruits attract animals to ingest fruit, swallow the seeds, and release them in the landscape, thus facilitating seed dispersal and plant regeneration. Attraction of animal dispersers is achieved via attractants such as color or scent, and rewards like sugars, lipids, and micronutrients. In addition to these attractants and rewards, a plethora of fruit and seed functional traits, including size, hardness, and chemistry, can affect the accessibility and attractiveness of fruits to seed‐dispersing animals. These functional traits form the interface between animals and fruits and, through trait matching, act as filters in dispersal networks. Yet, despite their critical roles in shaping seed dispersal networks, many fruit traits are not quantified in a standardized fashion, if they are quantified at all. As such, the existing databases of fruit traits used for syntheses lack many functional dimensions. We review the latest developments in fruit trait analysis, focusing on traits relevant for plant–frugivore interactions (i.e., morphology, color, chemistry), as well as some of their drivers (DNA, RNA, and microbial communities). We provide an overview of many existing methods, their advantages and disadvantages, and their application in field conditions.

Premise: Plants produce a tremendous variety of secondary compounds that are crucial to interspecific and intraspecific interactions and for adaptation to environmental changes. This chemical diversity has been attributed to multiple factors, including interactions with herbivores or pollinators, tissue‐specific needs, and evolutionary constraints. The interplay between a vast array of factors driving plant chemodiversity remains unclear, mainly because most studies have focused on a single organ—mostly leaves—or, when comparing different organs, have been limited to single taxa. Thus, the relationship between functional and phylogenetic factors remains unresolved. We use a model system of Ficus from Madagascar to examine the extent to which phytochemical diversity is shaped by tissue‐specific function and the degree to which phylogenetic relatedness explains variation in fruit and leaf chemodiversity.Methods: We applied an untargeted metabolomics approach to unripe fruits (the syconium, a hollow structure containing numerous small flowers) and leaves from eight species of wild figs (Ficus spp.) sampled in a tropical rainforest in Madagascar. We characterized their chemical profiles using ultra‐performance liquid chromatography–mass spectrometry and reconstructed their phylogeny using six genetic markers to understand the patterns of chemodiversity.Results: Fruit and leaf metabolomes were more similar to the same organ in other species than to the other organs within the same species. There was a significant but moderate phylogenetic correlation in fruit and leaf chemodiversity.Conclusions: Although phylogenetic relatedness influences plant chemodiversity in Malagasy figs, functional convergence of tissue‐specific metabolites may be a major evolutionary driver.

A paradigm in the plant defence literature is that defending against herbivores comes at a cost to growth, resulting in a growth–defence trade‐off. However, while there is strong evidence for growth–defence trade‐offs across species, evidence is mixed within species. Several mechanisms can account for this equivocal support within species, but teasing them apart requires examining growth–defence relationships both within and among populations, an approach seldom employed. We examined correlations between plant biomass (growth) and terpene production (defence) within and among populations of Monarda fistulosa, a perennial herb. We sampled populations from Montana and Wisconsin, regions that differ in resource availability characterized by different summer precipitation and associated abiotic conditions that influence plant productivity. We found negative, neutral and positive growth–defence correlations, depending on the scale examined. Negative correlations occurred across populations originating from divergent regions, positive correlations occurred across populations originating from within the high‐resource region and neutral correlations were found within single populations. Collectively, these results challenge the general expectation of ubiquitous trade‐offs and support emerging views that resource availability (as it affects productivity) shapes the evolution of defence at different scales. A free Plain Language Summary can be found within the Supporting Information of this article.