Understanding the Ecological Consequences of Phytochemical Diversity Through Molecular Networking Approaches
AuthorMcDermott, Kaitlin Marie
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Secondary metabolites are important mediators of a variety of biotic and abiotic interactions between plants and their surrounding environment. Many fully or partially characterized plants produce phytochemical mixtures that serve to protect the plant, including toxicity to herbivores. Despite the observed toxicity of secondary metabolites, some herbivores successfully specialize on toxic diets. Traditional methods for discovering/evaluating biologically active secondary metabolites in the context of organismal interactions have been targeted towards a specific set of compounds or compound classes. For partially characterized or uncharacterized plants, non-targeted metabolomic approaches are more desirable as they offer a more global evaluation of an organism’s metabolome, accounting for minor components and synergistic interactions. Current network approaches developed for large genomic datasets can be adapted to suit metabolomic datasets to separate significant trends from noise.Piper is a hyper-diverse plant genus that is well-known for its phytochemical diversity and chemically-mediated plant-insect interactions. The evolution of phytochemical diversity across a subset of Piper species in the Radula clade was investigated to test different phytochemical diversity hypotheses, specifically the co- evolutionary arms race and screening hypotheses. A cosine similarity scores network analysis revealed phytochemical diversity does not parallel species diversity. However, a weighted gene co-expression network analysis (WGCNA) suggested certain structural features and the corresponding biosynthetic pathways are conserved across the phylogeny. These results support the screening hypothesis where plants maintain high phytochemical diversity to increase their probability of producing a potent compound or precursor.The consequences of phytochemical diversity can also be applied to the mammalian herbivores Neotoma bryanti and N. lepida. N. bryanti and N. lepida are two closely related, yet geographically distinct, species whose habitats converge in a hybrid zone in Kelso Valley, CA. It is hypothesized that N. bryanti and N. lepida remain distinct by specializing on different toxic diets. A non-targeted metabolomic approach revealed N. bryanti and N. lepida have unique metabolic responses both when consuming their habitat-specific diets and when consuming the diet in the adjacent habitat. These findings suggest there are different metabolic strategies employed by the different species when consuming toxins they are not accustomed to in their normal diet. Furthermore, network analyses revealed the metabolic responses of these two species remain distinct despite seasonal changes in their diets. In addition, we found evidence of seasonal variation in gut microbial communities between N. bryanti and N. lepida, providing strong support that the gut microbiome is critically involved in the detoxification of various plant toxins encountered by these two species.Finally, we explored the consequences of milkweed (Asclepias) phytochemical diversity on the monarch butterfly (Danaus plexippus). Milkweed species are known to produce toxic cardiac glycosides, known as cardenolides, which have demonstrated anti- parasitic effects for the monarch butterfly. WGCNA of non-targeted metabolomic data resulted in the quantification of the chemotypes of two milkweed species, A. curassavica and A. incarnata. Careful inspection of these chemotypes revealed that flavonoids, in addition to cardenolides, may be an integral part of the monarch’s immune response.