Phylogenetic correlations among chemical and physical plant defenses change with ontogeny.

Theory predicts patterns of defense across taxa based on notions of tradeoffs and synergism among defensive traits when plants and herbivores coevolve. Because the expression of characters changes ontogenetically, the evolution of plant strategies may be best understood by considering multiple traits along a trajectory of plant development. Here we addressed the ontogenetic expression of chemical and physical defenses in 12 Datura species, and tested for macroevolutionary correlations between defensive traits using phylogenetic analyses. We used liquid chromatography coupled to mass spectrometry to identify the toxic tropane alkaloids of Datura, and also estimated leaf trichome density. We report three major patterns. First, we found different ontogenetic trajectories of alkaloids and leaf trichomes, with alkaloids increasing in concentration at the reproductive stage, whereas trichomes were much more variable across species. Second, the dominant alkaloids and leaf trichomes showed correlated evolution, with positive and negative associations. Third, the correlations between defensive traits changed across ontogeny, with significant relationships only occurring during the juvenile phase. The patterns in expression of defensive traits in the genus Datura are suggestive of adaptation to complex selective environments varying in space and time.

Herbivores can select for mixed defensive strategies in plants.

Resistance and tolerance are the most important defense mechanisms against herbivores. Initial theoretical studies considered both mechanisms functionally redundant, but more recent empirical studies suggest that these mechanisms may complement each other, favoring the presence of mixed defense patterns. However, the expectation of redundancy between tolerance and resistance remains unsupported. In this study, we tested this assumption following an ecological genetics field experiment in which the presence/absence of two herbivores (Lema daturaphila and Epitrix parvula) of Datura stramonium were manipulated. In each of three treatments, genotypic selection analyses were performed and selection patterns compared. Our results indicated that selection on resistance and tolerance was significantly different between the two folivores. Tolerance and resistance are not redundant defense strategies in D. stramonium but instead functioned as complementary defenses against both beetle species, favoring the evolution of a mixed defense strategy. Although each herbivore was selected for different defense strategies, the observed average tolerance and resistance were closer to the adaptive peak predicted against E. parvula and both beetles together. In our experimental population, natural selection imposed by herbivores can favor the evolution of mixed defense strategies in plants, accounting for the presence of intermediate levels of tolerance and resistance.