This content will become publicly available on August 23, 2024
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- Frontiers in Ecology and Evolution
- Medium: X
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- National Science Foundation
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Plants are often attacked by insects and other herbivores. As a result, they have evolved to defend themselves by producing many different chemicals that are toxic to these pests. As producing each chemical costs energy, individual plants often only produce one type of chemical that is targeted towards their main herbivore. Related species of plants often use the same type of chemical defense so, if a particular herbivore gains the ability to cope with this chemical, it may rapidly become an important pest for the whole plant family. To escape this threat, some plants have gained the ability to produce more than one type of chemical defense. Wallflowers, for example, are a group of plants in the mustard family that produce two types of toxic chemicals: mustard oils, which are common in most plants in this family; and cardenolides, which are an innovation of the wallflowers, and which are otherwise found only in distantly related plants such as foxglove and milkweed. The combination of these two chemical defenses within the same plant may have allowed the wallflowers to escape attacks from their main herbivores and may explain why the number of wallflower species rapidly increased within the last two million years. Züst et al. have now studied the diversity of mustard oils and cardenolides present in many different species of wallflower. This analysis revealed that almost all of the tested wallflower species produced high amounts of both chemical defenses, while only one species lacked the ability to produce cardenolides. The levels of mustard oils had no relation to the levels of cardenolides in the tested species, which suggests that the regulation of these two defenses is not linked. Furthermore, Züst et al. found that closely related wallflower species produced more similar cardenolides, but less similar mustard oils, to each other. This suggests that mustard oils and cardenolides have evolved independently in wallflowers and have distinct roles in the defense against different herbivores. The evolution of insect resistance to pesticides and other toxins is an important concern for agriculture. Applying multiple toxins to crops at the same time is an important strategy to slow the evolution of resistance in the pests. The findings of Züst et al. describe a system in which plants have naturally evolved an equivalent strategy to escape their main herbivores. Understanding how plants produce multiple chemical defenses, and the costs involved, may help efforts to breed crop species that are more resistant to herbivores and require fewer applications of pesticides.more » « less
Plant defense chemistry is often hypothesized to drive ecological and evolutionary success in diverse tropical forests, yet detailed characterizations of plant secondary metabolites in tropical plants are logistically challenging. Here, we explore a new integrative approach that combines visible‐to‐shortwave infrared (VSWIR) spectral reflectance data with detailed plant metabolomics data from 19
Protium(Burseraceae) tree species. Building on the discovery that different Protiumspecies have unique chemistries yet share many secondary metabolites, we devised a method to test for associations between metabolites and VSWIR spectral data. Given species‐level variation in metabolite abundance, we correlated the concentration of particular chemicals with the reflectance of the spectral bands in a wavelength band per secondary metabolite matrix. We included 45 metabolites that were shared by at least 5 Protiumspecies and correlated their per‐species foliar abundances against each one of 210 wavelength bands of field‐measured VSWIR spectra. Finally, we tested whether classes of similar metabolites showed similar relationships with spectral patterns. We found that many secondary metabolites yielded strong correlations with VSWIR spectra of Protium. Furthermore, important Protiummetabolite classes such as procyanidins (condensed tannins) and phytosterols were grouped together in a hierarchical clustering analysis (Ward’s algorithm), confirming similarity in their associations with plant spectral patterns. We also found a significant correlation in the phenolics content between juvenile and canopy trees of the same species, suggesting that species‐level variation in defense chemistry is consistent across life stages and geographic distribution. We conclude that the integration of spectral and metabolic approaches could represent a powerful and economical method to characterize important aspects of tropical plant defense chemistry.
Plant secondary metabolites are a key defence against herbivores, and their evolutionary origin is likely from primary metabolites. Yet for this to occur, an intermediate step of overexpression of primary metabolites would need to confer some advantage to the plant. Here, we examine the evolution of overexpression of the essential amino acid, L‐tyrosine and its role as a defence against herbivores.
We examined overexpression of tyrosine in 97 species of
Inga(Fabaceae), a genus of tropical trees, at five sites throughout the Neotropics. We predicted that tyrosine could act as an anti‐herbivore defence because concentrations of 4% tyrosine in artificial diets halved larval growth rates. We also collected insect herbivores to determine if tyrosine and its derivatives influenced host associations.
Overexpression of tyrosine was only present in a single lineage comprising 21 species, with concentrations ranging from 5% to 20% of the leaf dry weight. Overexpression was pronounced in expanding but not in mature leaves. Despite laboratory studies showing toxicity of L‐tyrosine,
Ingaspecies with tyrosine suffered higher levels of herbivory. We therefore hypothesize that overexpression is only favoured in species with less effective secondary metabolites. Some tyrosine‐producing species also contained secondary metabolites that are derived from tyrosine: tyrosine‐gallates, tyramine‐gallates and DOPA‐gallates. Elevated levels of transcripts of prephenate dehydrogenase, an enzyme in the tyrosine biosynthetic pathway that is insensitive to negative feedback from tyrosine, were found only in species that overexpress tyrosine or related gallates. Different lineages of herbivores showed contrasting responses to the overexpression of tyrosine and its derived secondary metabolites in their host plants. Synthesis. We propose that overexpression of some primary metabolites can serve as a chemical defence against herbivores, and are most likely to be selected for in species suffering high herbivory due to less effective secondary metabolites. Overexpression may be the first evolutionary step in the transition to the production of more derived secondary metabolites. Presumably, derived compounds would be more effective and less costly than free tyrosine as anti‐herbivore defences.
In coevolution between plants and insects, reciprocal selection often leads to phenotype matching between chemical defense and herbivore offense. Nonetheless, it is not well understood whether distinct plant parts are differentially defended and how herbivores adapted to those parts cope with tissue-specific defense. Milkweed plants produce a diversity of cardenolide toxins and specialist herbivores have substitutions in their target enzyme (Na + /K + –ATPase), each playing a central role in milkweed–insect coevolution. The four-eyed milkweed beetle ( Tetraopes tetrophthalmus ) is an abundant toxin-sequestering herbivore that feeds exclusively on milkweed roots as larvae and less so on milkweed leaves as adults. Accordingly, we tested the tolerance of this beetle’s Na + /K + –ATPase to cardenolide extracts from roots versus leaves of its main host ( Asclepias syriaca ), along with sequestered cardenolides from beetle tissues. We additionally purified and tested the inhibitory activity of dominant cardenolides from roots (syrioside) and leaves (glycosylated aspecioside). Tetraopes’ enzyme was threefold more tolerant of root extracts and syrioside than leaf cardenolides. Nonetheless, beetle-sequestered cardenolides were more potent than those in roots, suggesting selective uptake or dependence on compartmentalization of toxins away from the beetle’s enzymatic target. Because Tetraopes has two functionally validated amino acid substitutions in its Na + /K + –ATPase compared to the ancestral form in other insects, we compared its cardenolide tolerance to that of wild-type Drosophila and CRISPR-edited Drosophila with Tetraopes ’ Na + /K + –ATPase genotype. Those two amino acid substitutions accounted for >50% of Tetraopes’ enhanced enzymatic tolerance of cardenolides. Thus, milkweed’s tissue-specific expression of root toxins is matched by physiological adaptations in its specialist root herbivore.more » « less
Plant pathogens and herbivores can maintain forest diversity by reducing survival of tree seedlings close to conspecifics. However, how biogeographic variation in these natural enemies affects such distance‐dependent processes is unknown. Because invasive plants escape ecologically important enemies when introduced to a new range, distance‐dependent mortality may differ between their native and introduced ranges.
Here, we test whether the invasive tree
Triadica sebiferaescaped distance‐dependent mortality when introduced to the United States from China, and examine the roles of natural enemies in native and introduced ranges. In both the United States and China, we performed field surveys along with field and greenhouse experiments with field‐collected soils and soil sterilization treatments.
In field surveys and the field experiment, insect damage on
T. sebiferaseedlings decreased with distance to conspecific trees in the native range (China), but damage was low at all distances in the introduced range (United States). In the greenhouse experiment testing the effects of soil pathogens, T. sebiferaseedling mortality decreased with soil distance from conspecific trees in both ranges but distance‐independent mortality was higher in native range soils.
Our findings indicate that both insect herbivores and the soil biota contribute to distance‐dependent effects on
T. sebiferain its native range. They suggest, however, that plants may more readily escape herbivore than soil biota distance‐dependent effects when introduced to a new range and so herbivores, rather than soil pathogens, contribute more strongly to biogeographic variation in distance‐dependent effects. These results highlight the importance of considering species biogeographic variation in distance‐dependent effects and teasing apart the roles that different natural enemies play when studying species coexistence, community diversity and biological invasions.