Collaborative Research: Macroevolution of a group of plant secondary defense compounds (pyrrolizidine alkaloids) in the dogbane and milkweed flowering plant family (Apocynaceae)

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Plants are known to synthesize about 200,000 distinct secondary metabolites, chemical compounds that are not essential for their cellular metabolism. These plant secondary chemicals are important sources of medicines (e.g. aspirin), pesticides (e.g. pyrethrin), industrial compounds (e.g. latex), flavors (e.g. mint), and poisons (e.g. strychnine). To plants, these chemicals are essential defenses against herbivores, particularly insects. The efficacy of these defenses is not static over time, however, as herbivores adapt to their host plants defenses, evolving mechanisms to detoxify them or even co-opt them for their own defense against their predators. Thus a chemical that was once a valuable defense may become a liability, and its production lost. This project will investigate the evolution of a group of plant defense secondary compounds (pyrrolizidine alkaloids) in the dogbane and milkweed family (Apocynaceae). Plant secondary compounds in the Apocynaceae are diverse, with many having medicinal properties. Pyrrolizidine alkaloids in members of the Apocynaceae are highly toxic to non-adapted herbivores, but have little effect on specialist insects that store them within their tissues for defense against predators. Researchers will sample broadly across the Apocynaceae and reconstruct evolutionary relationships within the family using DNA sequence data. The resulting evolutionary tree will then be used as a framework to reconstruct the evolution of pyrrolizidine alkaloids within the group and better understand the relationship between these chemicals, the plants that produce them, and their herbivores. Undergraduate students will be trained in diverse molecular, evolutionary and biochemistry methods. Results from this project will also be integrated into undergraduate classes at three institutions, including two primarily undergraduate institutions. The research will provide new insights into evolutionary relationships within the medically important Apocynaceae plant family that can be used as a framework for broader questions within the family. An exhibit at the Academy of Natural Sciences in Philadelphia will broadly disseminate results from this research, and information on the broader topics of plant and insect defense, chemistry, and co-evolution, to the public. The overarching hypothesis to be tested in this research project proposes that the diversity of pyrrolizidine alkaloids will be lower in plant lineages that are highly exploited by insects immune to the effects of these compounds. To test this hypothesis researchers will use a combination of targeted enrichment and genome skimming (Hyb-Seq) to sequence ca. 850 low-copy nuclear loci, whole chloroplast genomes, and nuclear ribosomal genes, from 2 species of each of the 287 genera of the APSA clade (the lineage within Apocynaceae that includes most known milkweed butterfly host plants) to generate the required well-resolved and supported phylogeny and chronogram of the family. Researchers will then conduct a systematic survey of pyrrolizidine alkaloids occurrence in leaves across the APSA clade and reconstruct the evolution of both the pyrrolizidine alkaloids phenotype and of the underlying biosynthetic pathway, as well as expression and functional analyses in a subset of species. The origin of pyrrolizidine alkaloid biosynthesis in Apocynaceae will then be compared to the age of pyrrolizidine alkaloid co-option by Danainae, and test if the loss of pyrrolizidine alkaloids is correlated with host plant status.