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opencc-zeroApr 2023View details →

Data for: No physiological costs of dual sequestration of chemically different plant toxins in the milkweed bug Spilostethus saxatilis (Heteroptera: Lygaeidae)

Many herbivorous insects not only cope with plant toxins but also sequester them as a defense against predators and parasitoids. Sequestration is a product of the evolutionary arms race between plants and herbivorous insects and has been hypothesized to incur physiological costs due to specific adaptations required. Contradictory evidence about these costs exists for insects sequestering only one class of toxin, but very little is known about the physiological implications for species sequestering structurally different classes of compounds. Spilostethus saxatilis is a milkweed bug belonging to the cardenolide-sequestering heteropteran subfamily Lygaeinae (Heteroptera: Lygaeidae) that has shifted to the colchicine-containing plant Colchicum autumnale, a resource of chemically unrelated alkaloids. Using feeding-assays on artificial diet and chemical analysis, we assessed whether S. saxatilis is still able to sequester cardenolides apart from colchicine and related metabolites (colchicoids), and tested the effect of (1) either a natural cardenolide concentration (using ouabain as a model compound) or a natural colchicine concentration, (2) an increased concentration of both toxins, and (3) seeds of either Asclepias syriaca (cardenolides) or C. autumnale (colchicoids) on a set of life-history traits. For comparison, we assessed the same life-history traits in the milkweed bug Oncopeltus fasciatus exposed to cardenolides only. Although cardenolides and colchicoids have different physiological targets (Na+/K+-ATPase vs tubulin) and thus require different resistance traits, chronic exposure and sequestration of both isolated toxins caused no physiological costs such as reduced growth, increased mortality, lower fertility, or shorter adult life span in S. saxatilis. Indeed, an increased performance was observed in O. fasciatus and an according trend was found in S. saxatilis when feeding on isolated ouabain and isolated colchicine, respectively. Positive effects were even more pronounced when insects were provided with natural toxic seeds (i.e. C. autumnale for S. saxatilis and A. syriaca for O. fasciatus), especially in O. fasciatus. Our findings suggest, that S. saxatilis can sequester two chemically unrelated classes of plant compounds at a cost-free level, and that colchicoids may even play a beneficial role in terms of fertility.

opencc-zeroJul 2023View details →

The plant toxin 4-methylsulfinylbutyl isothiocyanate decreases herbivore performance and modulate cellular and humoral immunity

Insect herbivores frequently encounter plant defense molecules, but the physiological and ecological consequences for their immune systems are not fully understood. The majority of studies attempting to relate levels of plant defensive chemistry to herbivore immune responses have used natural population or species-level variation in plant defensive chemistry. Yet, this potentially confounds the effects of plant defense chemistry with other potential traits that may affect the expression of herbivore immunity such as development time and nutritional quality. We have used an artificial diet containing known quantities of a plant toxin (4-methylsulfinylbutyl isothiocyanate; 4MSOB-ITC or ITC), an isothiocyanate present in many plants in the genus Brassica, to explicitly explore the effects of a plant toxin on the cellular and humoral immune responses of the generalist herbivore Trichoplusia ni (Lepidoptera: Noctuidae) that frequently feeds on glucosinolate-containing plants. Caterpillars feeding on diets with high concentrations of ITC experienced reduced survivorship and growth rates. High concentrations of ITC suppressed the appearance of several types of hemocytes and melanization activity, which are critical defenses against parasitic Hymenoptera and microbial pathogens. In terms of T. ni humoral immunity, only the antimicrobial peptide (AMP) genes lebocin and gallerimycin were significantly upregulated in caterpillars fed on diets containing high levels of 4MSOB-ITC relative to caterpillars that were provided with ITC-free diet. Surprisingly, challenging caterpillars with a non-pathogenic strain of Escherichia coli resulted in the upregulation of the AMP gene cecropin. Feeding on high concentrations of plant toxins hindered caterpillar development and decreased cellular immunity but conferred mixed effects on humoral immunity. Our findings provide novel insights into the effects of herbivore diet composition on insect performance demonstrating the role of specific plant defense toxins that shape herbivore immunity and trophic interactions.

opencc-zeroJul 2023View details →

Late instar monarch caterpillars sabotage milkweed to acquire toxins, not to disarm plant defense

Sabotaging milkweed by monarch caterpillars (Danaus plexippus) is a famous textbook example of disarming plant defense. By severing leaf veins or petioles, monarchs are thought to prevent the flow of toxic latex to their feeding site. Here we show that sabotaging by monarch caterpillars is not only an avoidance strategy. While young caterpillars appear to avoid latex, late-instar caterpillars actively ingest exuding latex, presumably to increase sequestration of toxic latex cardenolides used for defense against predators. Comparisons with caterpillars of the related but non-sequestering common crow butterfly (Euploea core) revealed three lines of evidence supporting our hypothesis. First, monarch caterpillars sabotage inconsistently and therefore the behavior is not obligatory to feed on milkweed, whereas sabotaging precedes each feeding event in Euploea caterpillars. Second, monarch caterpillars shift their behavior from latex avoidance in younger stages to eager drinking in later stages, whereas Euploea caterpillars consistently avoid latex and spit it out during sabotaging. Third, monarchs reared on detached leaves without latex, sequestered more cardenolides when caterpillars imbibed latex offered with a pipette. Thus, we conclude that monarch caterpillars have transformed the 'sabotage to avoid' strategy of their relatives into a 'sabotage to consume' strategy implying a novel behavioral adaptation to increase sequestration of cardenolides for defense.

zenodo36/100

Data from "Tissue and toxin-specific divergent evolution in plant defense"

Files and code necessary to replicate the results from the manuscript are described as follows: Syrfampop.sas --> SAS code to conduct the analyses. HPLC_asyr.csv --> contains the cardenolide data of root, leaf and seed tissue from each individual plant belonging to multiple families of each of the two populations (main analysis in SAS code). chemmantelcorr.csv --> contains the correlation matrices between cardenolides within a given tissue (permutation test in SAS code) SS.csv --> contains the sums of squares matrices of cardenolide concentrations at the population and family levels for each tissue and whole plant after the MANOVA in the SAS code (used for the R code in Martin et al. (2008)). ehdbp.vcf --> Description of SNP data used for this study. ehdbp.arp --> SNP data in Arlequin format ready for FST analysis.

opencc-by-4.0Aug 2023View details →

publicApr 2023View details →

Data for: No physiological costs of dual sequestration of chemically different plant toxins in the milkweed bug Spilostethus saxatilis (Heteroptera: Lygaeidae)

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publicFeb 2024View details →

Late instar monarch caterpillars sabotage milkweed to acquire toxins, not to disarm plant defence

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publicJul 2023View details →

The plant toxin 4-methylsulfinylbutyl isothiocyanate decreases herbivore performance and modulate cellular and humoral immunity

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opencc-zeroAug 2020View details →

ABCB transporters in a leaf beetle respond to sequestered plant toxins

Phytophagous insects can tolerate and detoxify toxic compounds present in their host plants and have evolved intricate adaptations to this end. Some insects even sequester the toxins for their defense. This necessitates specific mechanisms, especially carrier proteins that regulate uptake and transport to specific storage sites or protect sensitive tissues from noxious compounds. We identified three ATP-binding cassette subfamily B (ABCB) transporters from the transcriptome of the cardenolide-sequestering leaf beetle Chrysochus auratus and analyzed their functional role in the sequestration process. These were heterologously expressed and tested for their ability to interact with various potential substrates: verapamil (standard ABCB substrate), the cardenolides digoxin (commonly used), cymarin (present in the species' host plant) and calotropin (present in the ancestral host plants). Verapamil stimulated all three ABCBs and each was activated by at least one cardenolide, however, they differed as to which they were activated by. While the expression of the most versatile transporter fits with a protective role in the blood-brain-barrier, the one specific for cymarin shows an extreme abundance in the elytra, coinciding with the location of the defensive glands. Our data thus suggest a key role of ABCBs in the transport network needed for cardenolide sequestration.

opencc-zeroDec 2014View details →

Data from: Spatial soil heterogeneity has a greater effect on symbiotic arbuscular mycorrhizal fungal communities and plant growth than genetic modification with Bacillus thuringiensis toxin genes

Maize, genetically modified with the insect toxin genes of Bacillus thuringiensis (Bt), is widely cultivated, yet its impacts on soil organisms are poorly understood. Arbuscular mycorrhizal fungi (AMF) form symbiotic associations with plant roots and may be uniquely sensitive to genetic changes within a plant host. In this field study, the effects of nine different lines of Bt maize and their corresponding non-Bt parental isolines were evaluated on AMF colonization and community diversity in plant roots. Plants were harvested 60 days after sowing, and data were collected on plant growth and per cent AMF colonization of roots. AMF community composition in roots was assessed using 454 pyrosequencing of the 28S rRNA genes, and spatial variation in mycorrhizal communities within replicated experimental field plots was examined. Growth responses, per cent AMF colonization of roots and AMF community diversity in roots did not differ between Bt and non-Bt maize, but root and shoot biomass and per cent colonization by arbuscules varied by maize cultivar. Plot identity had the most significant effect on plant growth, AMF colonization and AMF community composition in roots, indicating spatial heterogeneity in the field. Mycorrhizal fungal communities in maize roots were autocorrelated within approximately 1 m, but at greater distances, AMF community composition of roots differed between plants. Our findings indicate that spatial variation and heterogeneity in the field has a greater effect on the structure of AMF communities than host plant cultivar or modification by Bt toxin genes.

publicJun 2018View details →

Data from: Analysis of cytochrome P450 contribution to evolved plant toxin resistance in Drosophila sechellia

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publicMar 2017View details →

Data from: Plant toxin levels in nectar vary spatially across native and introduced populations

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publicMar 2015View details →

Data from: Spatial soil heterogeneity has a greater effect on symbiotic arbuscular mycorrhizal fungal communities and plant growth than genetic modification with Bacillus thuringiensis toxin genes

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publicApr 2021View details →

Different combinations of insect Na,K-ATPase α- and β-subunits enable fine-tuned adaptation to host plant toxins and tissue specific needs

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publicAug 2020View details →

ABCB transporters in a leaf beetle respond to sequestered plant toxins

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opencc-zeroDec 2014View details →

Data from: Population growth and sequestration of plant toxins along a gradient of specialization in four aphid species on the common milkweed Asclepias syriaca

Dietary specialization in insect herbivores has long been hypothesized to predict tolerance of plant defences, with more specialized herbivores being highly tolerant of and sometimes sequestering plant secondary compounds. Plant variation in secondary compounds should thus play an important and predictable role in shaping the performance and distribution of insect communities. We compared the performance of four naturally co-occurring aphid species on twenty genotypes of the common milkweed Asclepias syriaca. Genotypes of milkweed consistently differed in functional traits, including concentrations of toxic cardenolides, while the diet breadths of the four aphids ranged from broadly generalized to monophagous. The two more generalized species had the highest population growth rate overall, while growth rates decreased with increasing specialization. In contrast, honeydew exudation as a measure of phloem consumption increased with specialization; thus, resource-use efficiency was lower in specialist aphids. The two more generalized aphids grew best on genotypes with the highest plant growth rate (as an approximation for resource availability), while specialist aphids were not affected by plant growth. All four species contained apolar cardenolides in their bodies and excreted polar cardenolides, but only the most specialized aphid Myzocallis asclepiadis was negatively affected by increasing cardenolide concentrations of the host plant. Sequestration of cardenolides increased with diet specialization, with M. asclepiadis accumulating twice as much as any other species, perhaps explaining its susceptibility to plant cardenolides. Heritable plant traits differentially impacted co-occurring insect herbivores within the same guild. Generalist aphids were susceptible to variation in plant vigour but not defensive compounds. Increased host specialization resulted in lower resource-use efficiency, increased phloem throughput and ultimately higher cardenolide sequestration. Variation in these traits is thus likely to determine the relative distribution of generalist and specialist herbivores on plants in natural communities.

opencc-zeroAug 2019View details →

Data from: The role of volatile plant secondary metabolites as pre-ingestive cues and potential toxins dictating diet selection by African elephants

Understanding the factors driving diet selection represents one of the main thrusts of contemporary foraging ecology. Many studies have focussed on nutritional factors and anti-nutritional factors (such as tannins) that may describe diet selection of generalist mammalian herbivores, but these often do not explain the observed feeding patterns. Alternatively, generalist herbivores may be influenced by the presence, diversity, and/or concentration of toxins. Plant volatiles have been understudied, yet may play an important role in this context. We aimed to determine whether diet selection by African elephants is better correlated with the presence and concentration of toxic plant secondary metabolites (PSMs) than with nutritional or anti-nutritional factors. We also aimed to identify the specific aspects of the plant-odour profiles that were correlated with dietary selection, which could be used as a pre-ingestive cue for food selection. We found that elephant diet selection was not well described by crude protein, in vitro digestibility, tannin concentration, and total polyphenol concentration. Instead, the best predictors of elephant diet choice were the number and absolute (total) emissions of potentially toxic volatile PSMs, specifically monoterpenes. Elephants avoided plant species that emitted a wider diversity of volatile PSMs, had higher total emissions, and higher numbers and emissions of monoterpenes. This suggests that PSMs with a high propensity to become toxins, such as monoterpenes, are likely a better indicator for elephant diet avoidance than nutritional or anti-nutritional factors. Moreover, we demonstrated that elephants can differentiate between food items based on odour alone, specifically volatile monoterpenes, suggesting that these animals are relying on specific volatile cues emitted from plants to direct their foraging choices prior to ingesting selected plants.

opencc-zeroAug 2019View details →

Data from: New ways to acquire resistance – Imperfect convergence in insect adaptations to a potent plant toxin

Evolution of insensitivity to the toxic effects of cardiac glycosides has become a model in the study of convergent evolution, as five taxonomic orders of insects use the same few similar amino acid substitutions in the otherwise highly conserved Na,K-ATPase α. We here show that insensitivity in pyrgomorphid grasshoppers evolved along a slightly divergent path. As in other lineages, duplication of the Na,K-ATPase α gene paved the way for subfunctionalization: one copy maintains the ancestral, sensitive state while the other copy is resistant. Nonetheless, in contrast to all other investigated insects, the grasshoppers' resistant copy shows length variation by two amino acids in the first extracellular loop, the main part of the cardiac glycoside binding pocket. RT-qPCR analyses confirmed this copy is predominantly expressed in tissues exposed to the toxins, while the ancestral copy predominates in the nervous tissue. Functional tests with genetically engineered Drosophila Na,K-ATPases bearing the first extracellular loop of the pyrgomorphid genes showed the derived form to be highly resistant, while the ancestral state is sensitive. Thus, we report convergence in gene duplication and in the gene targets for toxin insensitivity, however the means to the phenotypic end have been novel in pyrgomorphid grasshoppers.