Ecological theory predicts that the high local diversity observed in tropical forests is maintained by negative density–dependent interactions within and between closely related plant species. By using long-term data on tree growth and survival for coexisting Inga (Fabaceae, Mimosoideae) congeners, we tested two mechanisms thought to underlie negative density dependence (NDD): competition for resources and attack by herbivores. We quantified the similarity of neighbors in terms of key ecological traits that mediate these interactions, as well as the similarity of herbivore communities. We show that phytochemical similarity and shared herbivore communities are associated with decreased growth and survival at the sapling stage, a key bottleneck in the life cycle of tropical trees. None of the traits associated with resource acquisition affect plant performance, indicating that competition between neighbors may not shape local tree diversity. These results suggest that herbivore pressure is the primary mechanism driving NDD at the sapling stage.
Cultivated maize (Zea mays) has retained much of the genetic diversity of its wild ancestors. Here, we performed nontargeted liquid chromatography-mass spectrometry metabolomics to analyze the metabolomes of the 282 maize inbred lines in the Goodman Diversity Panel. This analysis identified a bimodal distribution of foliar metabolites. Although 15% of the detected mass features were present in >90% of the inbred lines, the majority were found in <50% of the samples. Whereas leaf bases and tips were differentiated by flavonoid abundance, maize varieties (stiff-stalk, nonstiff-stalk, tropical, sweet maize, and popcorn) showed differential accumulation of benzoxazinoid metabolites. Genome-wide association studies (GWAS), performed for 3,991 mass features from the leaf tips and leaf bases, showed that 90% have multiple significantly associated loci scattered across the genome. Several quantitative trait locus hotspots in the maize genome regulate the abundance of multiple, often structurally related mass features. The utility of maize metabolite GWAS was demonstrated by confirming known benzoxazinoid biosynthesis genes, as well as by mapping isomeric variation in the accumulation of phenylpropanoid hydroxycitric acid esters to a single linkage block in a citrate synthase-like gene. Similar to gene expression databases, this metabolomic GWAS data set constitutes an important public resource for linking maize metabolites with biosynthetic and regulatory genes.
Coevolutionary theory has long predicted that the arms race between plants and herbivores is a major driver of host selection and diversification. At a local scale, plant defenses contribute significantly to the structure of herbivore assemblages and the high alpha diversity of plants in tropical rain forests. However, the general importance of plant defenses in host associations and divergence at regional scales remains unclear. Here, we examine the role of plant defensive traits and phylogeny in the evolution of host range and species divergence in leaf-feeding sawflies of the family Argidae associated with Neotropical trees in the genus Inga throughout the Amazon, the Guiana Shield and Panama. Our analyses show that the phylogenies of both the sawfly herbivores and their Inga hosts are congruent, and that sawflies radiated at approximately the same time, or more recently than their Inga hosts. Analyses controlling for phylogenetic effects show that the evolution of host use in the sawflies associated with Inga is better correlated with Inga chemistry than with Inga phylogeny, suggesting a pattern of delayed host tracking closely tied to host chemistry. Finally, phylogenetic analyses show that sister species of Inga-sawflies are dispersed across the Neotropics, suggesting a role for allopatric divergence and vicariance in Inga diversification. These results are consistent with the idea that host defensive traits play a key role not only in structuring the herbivore assemblages at a single site, but also in the processes shaping host association and species divergence at a regional scale.
Many plants produce structurally related defensive metabolites with the same target sites in insect herbivores. Two possible drivers of this chemical diversity are: (i) interacting effects of structurally related compounds increase resistance against individual herbivores, and (ii) variants of the same chemical structures differentially affect diverse herbivore species or feeding guilds. Erysimum cheiranthoides L (Brassicaceae; wormseed wallflower) produces abundant and diverse cardenolide toxins, which are derived from digitoxigenin, cannogenol, and strophanthidin, all of which inhibit Na + /K +-ATPases in animal cells. Here we describe an E. cheiranthoides mutant with 66% lower cardenolide content, resulting from greatly decreased cannogenol-and strophanthidin-derived cardenolides, partially compensated for by increases in digitoxigenin-derived cardenolides. This compositional change created a more even cardenolide distribution, decreased the average cardenolide polarity, but did not impact glucosinolates, a different class of chemical defenses. Growth of generalist herbivores from two feeding guilds, Myzus persicae Sulzer (Hemiptera: Aphididae; green peach aphid) and Trichoplusia ni Hübner (Lepidoptera: Noctuidae; cabbage looper), was decreased on the mutant line compared to wildtype. Both herbivores accumulated cardenolides in proportion to plant content, with T. ni accumulating higher total concentrations than M. persicae. Helveticoside, an abundant cardenolide in E. cheiranthoides, was absent in M. persicae, suggesting that this compound is not present in the phloem. Our results support the hypothesis that cardenolide diversity protects plants against different herbivores, with digitoxigenin-derived compounds providing better protection against insects like M. persicae and T. ni, whereas cannogenol and strophanthidin provide better protection against other herbivores of E. cheiranthoides.
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