Phylogenetic analysis of secondary metabolites in a plant community provides evidence for trade-offs between biotic and abiotic stress tolerance

Abstract

Plants' responses to conflicting stresses may result in physiological trade-offs due to the inter-dependent and costly nature of physiological investments. Physiological tradeoffs have been proved within species, but to what extent these trade-offs are the result of phylogenetic constraints remains poorly known. Environmental stresses can vary widely in different biomes, and therefore assessing physiological tradeoffs across species must account for this variation. One way of doing so is to assess it within a community, where the co-occurring species have faced a shared combination of filters to establish. Considering a representative sample of species in a single community, we use a macroevolutionary approach to test the hypothesis that plant physiological trade-offs are evolutionarily conserved within this community (i.e., closely-related species tend to solve the trade-offs similarly). We analyze the content of five metabolites in thirty co-occurring plant species, capturing their range of contrasting exposures to abiotic and biotic stresses (growing solitary and in vegetation patches). Our results support that species investment in response to abiotic stress (i.e., proline and abscisic acid content) is traded off against their investment to face biotic stress (i.e., jasmonic acid and salicylic acid), shown by the contrasting loadings of these two groups of metabolites in the first axes of a principal component analysis (PCA). In addition, the metabolic strategies observed in this community are evolutionarily conserved, as closely related species tend to have similar scores in this PCA, and thus resemble each other in their balance. This is shown by a significant phylogenetic signal in the species’ scores along the first axes of the PCA. Incorporating the evolutionary history of plant species into physiological studies can help to understand the response of plants to multiple stresses currently acting in ecological communities.