Evidence for both phylogenetic conservatism and lability in the evolution of secondary chemistry in a tropical angiosperm radiation

Over evolutionary timescales, shifts in plant secondary chemistry may be associated with patterns of diversification in associated arthropods. Although foundational hypotheses of plant-insect codiversification and plant defense theory posit closely related plants should have similar chemical profiles, numerous studies have documented variation in the degree of phylogenetic signal, suggesting phytochemical evolution is more nuanced than initially assumed. We utilize proton nuclear magnetic resonance (1H NMR) data, chemical classification, and genotyping-by-sequencing to resolve evolutionary relationships and characterize the evolution of secondary chemistry in the Neotropical plant clade Radula (Piper; Piperaceae). Sequencing data substantially improved phylogenetic resolution relative to past studies, and spectroscopic characterization revealed the presence of 35 metabolite classes. Broad metabolite classes displayed strong phylogenetic signal, whereas the crude 1H NMR spectra featured evolutionary lability in chemical resonances. Evolutionary correlations were detected in two pairs of compound classes (flavonoids with chalcones; p-alkenyl phenols with kavalactones), where the gain or loss of a class was dependent on the others state. Overall, the evolution of secondary chemistry in Radula is characterized by strong phylogenetic signal of broad compound classes and concomitant evolutionary lability of specialized chemical motifs, consistent with both classic evolutionary hypotheses and recent examinations of phytochemical evolution in young lineages.