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1. A test of the Geographic Mosaic Theory of Coevolution: investigating widespread species of Amazonian Protium (Burseraceae) trees, their chemical defenses, and their associated herbivore faunas

   https://doi.org/10.3389/fevo.2023.1180274  

   Fine, Paul V.; Baccaro, Fabricio Beggiato; Lokvam, John; Mesones, Italo; Vásquez Pilco, Magno; Ayarza Zuñiga, J. Milagros; Merkel, Emerson; Sanches, Marcelle; Nogueira, Carlos A.; Salazar, Diego (August 2023, Frontiers in Ecology and Evolution)

   Introduction Plants and their insect herbivores represent a large fraction of the species in Amazonian forests and are often directly implicated in the origin and maintenance of biodiversity at local and regional scales. How these interactions may change over geographic distance is unknown because very few studies have investigated the herbivore fauna and defense chemicals of any host plant species at multiple sites in tropical forests. One hypothesis, the Geographic Mosaic Theory of Coevolution, predicts that if herbivore assemblages turn over in different parts of a plant’s range, then plant defense chemicals should also change, reflecting local selection pressures. Methods We tested this theory by studying 12 species of Protium (Burseraceae) trees that occur in both Iquitos, Peru, and Manaus, Brazil, in rainforests separated by 1500 km. We surveyed all insects observed directly feeding on the plants in both locations for 48 weeks in Manaus and 64 weeks in Iquitos. We analyzed the secondary metabolites in the leaves of all species in both locations using GC/MS and HPLC. Results and Discussion Although in both locations we found that Protium herbivores were dominated by insects from the orders Hemiptera, Coleoptera and Lepidoptera, we found almost complete turnover in the herbivore species composition in the two sites, and each host plant species had a different assemblage of herbivores in each location. Comparing the phylogenetic beta-diversity, we found low similarity in herbivore phylogenetic relatedness between host plant species in the two locations. However, the secondary metabolites found within a Protium species were similar across the two locations. We found no strong evidence that individuals from a host plant species in Iquitos or Manaus expressed locally-adapted defense chemicals, as individuals from geographic locations did not form clusters when looking at patterns of chemical similarity. These results are not consistent with the Geographic Mosaic Theory of Coevolution. The most intriguing pattern we found was a strong correlation between the diversity of herbivores per host plant species in both locations. We also found that plants with high chemical richness had lower numbers of herbivore species and numbers of total herbivores in both locations. We conclude that high chemical diversity is the most effective strategy for Protium trees to reduce insect herbivore attacks. We speculate that each secondary metabolite is effective at repelling only a few insect herbivores, and that different chemicals are likely effective in different parts of a plants’ geographic range. Future studies should investigate additional locations and additional natural enemies (i.e., fungal pathogens) to test the hypothesis that chemical diversity reduces attack from natural enemies and may explain the ecological and evolutionary success of rainforest trees over time and space. 

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2. Independent evolution of ancestral and novel defenses in a genus of toxic plants (Erysimum, Brassicaceae)

   https://doi.org/10.7554/eLife.51712  

   Züst, Tobias; Strickler, Susan R; Powell, Adrian F; Mabry, Makenzie E; An, Hong; Mirzaei, Mahdieh; York, Thomas; Holland, Cynthia K; Kumar, Pavan; Erb, Matthias; et al (April 2020, eLife)

   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. 

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3. Variation in immune response in the generalist herbivore fall webworm across four common host plants

   https://doi.org/10.1111/eea.13502  

   Mitchell, Audrey M; Vyas, Dhaval K; Murphy, Shannon M (November 2024, Entomologia Experimentalis et Applicata)

   Abstract Dietary generalist herbivorous insects are widespread and often occur in a variety of environments. Across their geographic range, herbivorous insects may encounter variable plant traits as they feed on high‐quality or low‐quality plants. Herbivorous insect larvae experience both bottom‐up (host plant) and top‐down (parasitoid) factors that affect survival. Host plant quality may affect larval growth and survival in that larvae feeding on low‐quality plants often suffer reduced fitness. However, herbivores on different host plants are also subject to different levels of parasitism. High‐quality plants confer stronger larval performance (higher survival, more offspring), but larvae may also face higher parasitism. In some herbivore species, diet mediates larval immune response. The generalist insect herbivore fall webworm (FW),Hyphantria cuneaDrury (Lepidoptera: Erebidae), is a moth native to North America, and its larvae have considerable variance in their performance when reared on different host plants. We investigated whether diet affects the immune response in FW larvae when they are reared on different host plant species known to vary in food quality. We measured immune response by melanization of a nylon filament. We found significant differences in immune response across host plants, indicating that diet mediates immune response in FW larvae. Our study helps elucidate the factors that cause variation in immune response in a generalist herbivore. 

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4. Tissue-specific plant toxins and adaptation in a specialist root herbivore

   https://doi.org/10.1073/pnas.2302251120  

   Agrawal, Anurag A.; Hastings, Amy P. (May 2023, Proceedings of the National Academy of Sciences)

   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. 

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5. Use of an exotic host plant shifts immunity, chemical defense, and viral burden in wild populations of a specialist insect herbivore

   https://doi.org/10.1002/ece3.8723  

   Muchoney, Nadya D.; Bowers, M. Deane; Carper, Adrian L.; Mason, Peri A.; Teglas, Mike B.; Smilanich, Angela M. (March 2022, Ecology and Evolution)

   Abstract Defense against natural enemies constitutes an important driver of herbivore host range evolution in the wild. Populations of the Baltimore checkerspot butterfly,Euphydryas phaeton(Nymphalidae), have recently incorporated an exotic plant,Plantago lanceolata(Plantaginaceae), into their dietary range. To understand the tritrophic consequences of utilizing this exotic host plant, we examined immune performance, chemical defense, and interactions with a natural entomopathogen (Junonia coenia densovirus,Parvoviridae) across wild populations of this specialist herbivore. We measured three immune parameters, sequestration of defensive iridoid glycosides (IGs), and viral infection load in field‐collected caterpillars using eitherP.lanceolataor a native plant,Chelone glabra(Plantaginaceae). We found that larvae using the exotic plant exhibited reduced immunocompetence, compositional differences in IG sequestration, and higher in situ viral burdens compared to those using the native plant. On both host plants, high IG sequestration was associated with reduced hemocyte concentration in the larval hemolymph, providing the first evidence of incompatibility between sequestered chemical defenses and the immune response (i.e., the “vulnerable host” hypothesis) from a field‐based study. However, despite this negative relationship between IG sequestration and cellular immunity, caterpillars with greater sequestration harbored lower viral loads. While survival of virus‐infected individuals decreased with increasing viral burden, it ultimately did not differ between the exotic and native plants. These results provide evidence that: (1) phytochemical sequestration may contribute to defense against pathogens even when immunity is compromised and (2) herbivore persistence on exotic plant species may be facilitated by sequestration and its role in defense against natural enemies. 

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