Abstract
Floral scent is a key communication channel between plants and pollinators. However, the contributions of environment and phylogeny to floral scent composition remain poorly understood. In this study, we characterized interspecific variation of floral scent composition in the genus Jaborosa Juss. (Solanaceae) and, using an ecological niche modelling approach (ENM), we assessed the environmental variables that exerted the strongest influence on floral scent variation, taking into account pollination mode and phylogenetic relationships. Our results indicate that two major evolutionary themes have emerged: (i) a ‘warm Lowland Subtropical nectar-rewarding clade’ with large white hawkmoth pollinated flowers that emit fragrances dominated by oxygenated aromatic or sesquiterpenoid volatiles, and (ii) a ‘cool-temperate brood-deceptive clade’ of largely fly-pollinated species found at high altitudes (Andes) or latitudes (Patagonian Steppe) that emit foul odors including cresol, indole and sulfuric volatiles. The joint consideration of floral scent profiles, pollination mode, and geoclimatic context helped us to disentangle the factors that shaped floral scent evolution across “pollinator climates” (geographic differences in pollinator abundance or preference). Our findings suggest that the ability of plants in the genus Jaborosa to colonize newly formed habitats during Andean orogeny was associated with striking transitions in flower scent composition that trigger specific odor-driven behaviors in nocturnal hawkmoths and saprophilous fly pollinators.
Highlights
IntroductionChemical communication via floral scent plays a central role in attracting pollinators and is considered a key innovation promoting pollinator shifts and diversification in flowering plants [1,2,3]
Four environmental variables were highly associated with PC1 scores: one positively (altitude (40%)), and three negatively
The flowers of most Jaborosa species smelled strongly to our human noses for entirely different reasons; hawkmoth-pollinated flowers of the Subtropical Lowland clade emit large amounts of common and inoffensive scent compounds, whereas fly-pollinated flowers of the Andean clade emit low amounts of pungent, fetid compounds to which the human nose is highly sensitive. This distinction, which highlights key differences in the chemical structures and properties of the volatile organic compounds (VOCs) associated with hawkmoth vs. fly pollination, compelled us to utilize three different methods in order to ensure that we could detect specific compounds across our sampled species
Summary
Chemical communication via floral scent plays a central role in attracting pollinators and is considered a key innovation promoting pollinator shifts and diversification in flowering plants [1,2,3]. Floral scent combines with non-chemical components of floral display in complex, multi-sensory communication between flowers and their animal visitors [4,5,6]. Floral scent itself can be considered as a multichannel signal, and small evolutionary changes in scent composition may open (or close) signal channels for certain flower visitors that directly affect plant fitness [7,8,9]. Pollinator olfactory sensory acuity and olfactory learning are important components of the selective environment that shape floral evolution in angiosperms [10,11,12]
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