Diversity and divergence: evolution of secondary metabolism in the tropical tree genus Inga.

Plants are widely recognized as chemical factories, with each species producing dozens to hundreds of unique secondary metabolites. These compounds shape the interactions between plants and their natural enemies. We explore the evolutionary patterns and processes by which plants generate chemical diversity, from evolving novel compounds to unique chemical profiles. We characterized the chemical profile of one-third of the species of tropical rainforest trees in the genus Inga (c. 100, Fabaceae) using ultraperformance liquid chromatography-mass spectrometry-based metabolomics and applied phylogenetic comparative methods to understand the mode of chemical evolution. We show: each Inga species contain structurally unrelated compounds and high levels of phytochemical diversity; closely related species have divergent chemical profiles, with individual compounds, compound classes, and chemical profiles showing little-to-no phylogenetic signal; at the evolutionary time scale, a species' chemical profile shows a signature of divergent adaptation. At the ecological time scale, sympatric species were the most divergent, implying it is also advantageous to maintain a unique chemical profile from community members; finally, we integrate these patterns with a model for how chemical diversity evolves. Taken together, these results show that phytochemical diversity and divergence are fundamental to the ecology and evolution of plants.

Phenolics lie at the centre of functional versatility in the responses of two phytochemically diverse tropical trees to canopy thinning.

Saplings in the shade of the tropical understorey face the challenge of acquiring sufficient carbon for growth as well as defence against intense pest pressure. A minor increase in light availability via canopy thinning may allow for increased investment in chemical defence against pests, but it may also necessitate additional biochemical investment to prevent light-induced oxidative stress. The shifts in secondary metabolite composition that increased sun exposure may precipitate in such tree species present an ideal milieu for evaluating the potential of a single suite of phenolic secondary metabolites to be used in mitigating both abiotic and biotic stressors. To conduct such an evaluation, we exposed saplings of two unrelated species to a range of light environments and compared changes in their foliar secondary metabolome alongside corresponding changes in the abiotic and biotic activity of their secondary metabolite suites. Among the numerous classes of secondary metabolites found in both species, phenolics accounted for the majority of increases in antioxidant and UV-absorbing properties as well as activity against an invertebrate herbivore and a fungal pathogen. Our results support the hypothesis that phenolics contribute to the capacity of plants to resist co-occurring abiotic and biotic stressors in resource-limited conditions.