The evolution of fruit scent: phylogenetic and developmental constraints

Omer Nevo,Juan Antonio James Jeffrey,Diary Razafimandimby,Annemarie Kleiner,Kim Valenta,Manfred Ayasse,Colin A Chapman

doi:10.1186/s12862-020-01708-2

Abstract

BackgroundFruit scent is increasingly recognized as an evolved signal whose function is to attract animal seed dispersers and facilitate plant reproduction. However, like all traits, fruit scent is likely to evolve in response to conflicting selective pressures and various constraints. Two major constraints are (i) phylogenetic constraints, in which traits are inherited from ancestors rather than adapted to current conditions and (ii) developmental constraints, if phenotypes are limited by the expression of other traits within the individual. We tested whether phylogenetic constraints play a role in fruit scent evolution by calculating the phylogenetic signal in ripe fruits of 98 species from three study sites. We then estimated the importance of developmental constraints by examining whether ripe fruits tend to emit compounds that are chemically similar to, and share biosynthetic pathways with, compounds emitted by conspecific unripe fruits from which they develop.ResultsWe show that closely related taxa are not more similar to each other than to very distinct taxa, thus indicating that fruit scent shows little phylogenetic signal. At the same time, although ripe and unripe fruits of the same species tend to emit different chemicals, they tend to employ chemicals originating from similar biosynthetic pathways, thus indicating that some developmental constraints determine ripe fruit scent.ConclusionsOur results highlight the complex landscape in which fruit scent has evolved. On one hand, fruit scent evolution is not limited by common ancestry. On the other hand, the range of chemicals that can be employed in ripe fruits is probably constrained by the needs of unripe fruits.

Highlights

Fruit scent is increasingly recognized as an evolved signal whose function is to attract animal seed dispersers and facilitate plant reproduction
To evaluate whether fruit scent is constrained by developmental constraints, we examine whether ripe fruit Volatile organic compound (VOC) profile resembles conspecific unripe fruits in a subset of 30 species from one study site, from which we had data for unripe fruits
Phylogenetic constraints In all three systems, we found no phylogenetic signal at either the compound or class level, indicating that ripe fruit scent is not explained by common ancestry (Table 1; Additional file 1: Fig. S1, Additional file 2: Fig. S2, Additional file 3: Fig. S3)

Summary

Introduction

Fruit scent is increasingly recognized as an evolved signal whose function is to attract animal seed dispersers and facilitate plant reproduction. We tested whether phylogenetic constraints play a role in fruit scent evolution by calculating the phylogenetic signal in ripe fruits of 98 species from three study sites. Fig scent has been found to function as an attractant to seed dispersing bats in various species in both. It has been shown that fruits of species that specialize on seed dispersal by lemurs have evolved to signal ripeness [18] and even nutrient content [22, 23] through scent, and that fruit scent plays a major role in the food acquisition strategies of capuchin monkeys [20]. There is a growing acknowledgment that fruit scent functions as a communication system between plants and seed dispersers

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