Abstract
Foundational hypotheses addressing plant–insect codiversification and plant defense theory typically assume a macroevolutionary pattern whereby closely related plants have similar chemical profiles. However, numerous studies have documented variation in the degree of phytochemical trait lability, raising the possibility that phytochemical evolution is more nuanced than initially assumed. We utilize proton nuclear magnetic resonance (1H NMR) data, chemical classification, and double digest restriction-site associated DNA sequencing (ddRADseq) 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. Metabolite classes displayed phylogenetic signal, whereas the crude 1H NMR spectra featured little evidence of phylogenetic signal in multivariate tests of 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 other’s state. Overall, the evolution of secondary chemistry in Radula is characterized by strong phylogenetic signal of traditional compound classes and weak phylogenetic signal of specialized chemical motifs, consistent with both classic evolutionary hypotheses and recent examinations of phytochemical evolution in young lineages.
Highlights
Foundational hypotheses addressing plant–insect codiversification and plant defense theory typically assume a macroevolutionary pattern whereby closely related plants have similar chemical profiles
After contaminant filtering and demultiplexing, we retained ~ 313 million Illumina reads for phylogenetic analyses
There are numerous limitations that could affect estimates of phylogenetic signal in comparative studies[54] that are relevant to the analyses presented here
Summary
Foundational hypotheses addressing plant–insect codiversification and plant defense theory typically assume a macroevolutionary pattern whereby closely related plants have similar chemical profiles. The evolution of secondary chemistry in Radula is characterized by strong phylogenetic signal of traditional compound classes and weak phylogenetic signal of specialized chemical motifs, consistent with both classic evolutionary hypotheses and recent examinations of phytochemical evolution in young lineages. Numerous studies provide evidence for evolutionary lability in chemical traits within genera[7,14,15,16], suggesting that surveys of phytochemical variation within young plant lineages might yield variable perspectives on the evolution of secondary chemistry. Johnson et al.[18] found a strong positive correlation between flavonoids and phenolic diversity and a strong negative correlation between ellagitannins and flavonoids across a phylogeny of 26 evening primroses (Oenethera: Onagraceae) Such associations are relevant because they may reflect evolutionary constraints, and their causes may be varied. Approaches that capture a larger proportion of the structural variation underlying phytochemical phenotypes could be well suited to addressing hypotheses concerning evolutionary patterns
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