Insect adaptations toward plant toxins in milkweed–herbivores systems – a review

Birnbaum, Stephanie S.L.; Abbot, Patrick

doi:10.1111/eea.12659

Cited by 30 publications

(30 citation statements)

References 103 publications

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“…Among these milkweed herbivores, sequestration of cardenolides is often linked to the gain of target‐site insensitivity in the otherwise highly conserved Na + /K + ‐ATPase enzyme (Dobler et al., ; Zhen, Aardema, Medina, Schumer, & Andolfatto, ); in fact, the defensive benefit from cardenolide sequestration may have been a key evolutionary driver of target‐site insensitivity (Petschenka & Agrawal, ). As a prominent exception among cardenolide‐sequestering herbivores, A. nerii lacks a resistant Na + /K + ‐ATPase (Zhen et al., ), and instead may primarily rely on cardenolide detoxification (Birnbaum & Abbot, ; Birnbaum, Rinker, Gerardo, & Abbot, ). Furthermore, while sequestration of cardenolides in most herbivores involves at least partially active uptake (Dobler et al., ), sequestration by A. nerii appears to be primarily passive (Züst & Agrawal, 2016b).…”

Section: Introductionmentioning

confidence: 99%

What doesn’t kill you makes you stronger: The burdens and benefits of toxin sequestration in a milkweed aphid

2018

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Specialized insect herbivores commonly co‐opt plant defences for protection against predators, but the costs, benefits and mechanisms of sequestration are poorly understood. We quantified sequestration of toxic cardenolides by the specialist aphid Aphis nerii when reared on four closely related milkweed (Asclepias) species with >20‐fold variation in cardenolide content, and in the presence or absence of generalist ladybug predators. Increasing concentrations of apolar plant cardenolides increased sequestered amounts in aphids. High concentrations in plants impaired aphid population growth, but also reduced the top‐down effects of predators. An in vitro enzymatic assay of total cardenolides in aphid bodies using the cardenolides’ target (animal Na+/K+‐ATPase) revealed that the subset of sequestered cardenolides is disproportionally more toxic than cardenolides in leaves. All aphids accumulated two cardenolides not present in their host plant, even on plants with very low foliar cardenolide concentrations. Sequestration of potent cardenolides by A. nerii thus involves passive, concentration‐dependent uptake from the host plant, as well as a presumably more active mechanism of modification and up‐concentration of plant cardenolides. The concentration of toxins in the host plant thus not only determines the negative impacts on growth and performance of an aphid, but also the ease and efficiency by which toxins are sequestered for the aphid’s defence, making the costs and benefits of plant toxins highly context‐dependent for both the plant and the herbivore. Therefore, variation in plant toxins is of central importance for co‐evolutionary plant–insect interactions, particularly in environments with variable predator pressure. A http://onlinelibrary.wiley.com/doi/10.1111/1365-2435.13144/suppinfo is available for this article.

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Section: Introductionmentioning

confidence: 99%

What doesn’t kill you makes you stronger: The burdens and benefits of toxin sequestration in a milkweed aphid

2018

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“…Research over the past several decades has shown that the molecular adaptations of herbivorous insects to plant toxins mainly involve toxin degradation (metabolic adaptation) and target-site mutations (Salunke et al, 2005;Sun et al, 2006;Misra et al, 2011). Generally, metabolic adaptations of insects, in the most common strategy via biotransformation of plant toxins, include phases I, II, and III mechanisms (Després et al, 2007;Birnbaum and Abbot, 2018). These three metabolic mechanisms are involved in many detoxification enzymes, such as cytochrome P450s, carboxylesterases, glutathione-S-transferases (GSTs), and uridine diphosphate (UDP)-glycosyltransferases (UGTs).…”

Section: Discussionmentioning

confidence: 99%

“…Aside from metabolic adaptations, many insect species have evolved "target-site modifications" at the binding location of toxins to protect themselves from plant toxic compounds (Després et al, 2007;Zhen et al, 2012;Ujvari et al, 2015). In addition, some gut microbes in insects can play important roles in the detoxification of toxic compounds (Henry et al, 2013;Giron et al, 2017;Birnbaum and Abbot, 2018). However, whether these mechanisms were also involved in the resistance of grasshoppers to rutin should be studied in the future.…”

Section: Discussionmentioning

confidence: 99%

Phenotypic and Transcriptomic Response of the Grasshopper Oedaleus asiaticus (Orthoptera: Acrididae) to Toxic Rutin

Huang

Zhang

et al. 2020

Front. Physiol.

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Rutin, a widely distributed phytochemical flavonoid, can be used to control insect pests. In this study, we studied the growth performance of the grasshopper Oedaleus asiaticus Bey-Bienko given xenobiotic rutin using feeding experiments and transcriptomic analysis. O. asiaticus had reduced body size, lower survival rate, and reduced growth performance when fed with xenobiotic rutin. Rutin-fed nymphs had large variation in gene expression profiles, with a total of 308 genes significantly upregulated and 287 genes downregulated. The upregulated genes were significantly enriched in stress resistance-, immune-, and detoxification-related biological processes and the Kyoto Encyclopedia of Genes and Genomes (KEGG) pathways. Downregulated genes mainly involved cuticle biosynthesis and nutrition metabolism-related pathways. The quantitative real-time PCR (qRT-PCR) analysis of 15 candidate genes also produced results consistent with the transcriptome data. These results suggested that grasshoppers' capacity for biosynthesis and nutrition metabolism decreased, and stress resistance and metabolized capacity to toxic substances were significantly induced when O. asiaticus was fed on xenobiotic rutin. Rutin, as a phytotoxin, had detrimental effects and induced changes in gene expression profiles for O. asiaticus. This study can provide a molecular basis and offer future opportunities for the development of rutin-related insecticides and their application to grasshopper control.

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“…A frequent argument for why plant defenses affect the evolution of insect herbivores is the negative correlation between the degree of plant toxicity and the number of insect herbivores that can thrive under such toxicity (Ehrlich & Raven, 1964;Fox & Morrow, 1981;Rasmann & Agrawal, 2011). For example, plants in the genus Asclepias produce cardenolides and latex as defensive mechanisms and only a handful of insects (c. 12) are able to feed on them (Agrawal et al, 2008(Agrawal et al, , 2012Rasmann, 2014;Birnbaum & Abbot, 2018). Thus, specialization and costs of specific adaptations are implied as important influences in the evolution of herbivores (Karageorgi et al, 2019).…”

Section: Introductionmentioning

confidence: 99%

“…Thus, specialization and costs of specific adaptations are implied as important influences in the evolution of herbivores (Karageorgi et al, 2019). Variation in these adaptive traits among milkweed insects makes them an excellent system to study plant-herbivore co-evolution and the role that plant defenses play in insect specialization (Price & Wilson, 1979;Van Zandt & Agrawal, 2004;Birnbaum & Abbot, 2018).…”

Section: Introductionmentioning

confidence: 99%

Host specificity and variation in oviposition behaviour of milkweed stem weevils and implications for species divergence

Hernández

Davis

Agrawal

2020

Ecological Entomology

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1. An herbivore's life‐history strategy, including optimization of resource use, is constrained by its evolutionary history and ecological factors varying across the landscape. 2. We asked if related and co‐distributed herbivore species maintain consistency of host preference and oviposition behaviours along the species' range. We surveyed two putative species of milkweed stem weevils, Rhyssomatus lineaticollis and R. annectens, which co‐occur alongside their hosts, Asclepias syriaca and A. incarnata. 3. We confirmed the two species status of weevils, supported by differences in morphology and a bilocus gene phylogeny. Furthermore, we found that species divergence recapitulated the weevils current host plant use. 4. We found oviposition variation within and between species. R. annectens poked the stem haphazardly or girdled it before oviposition. Meanwhile, R. lineaticollis primarily trenched stems in the north, but poked or girdled in the south. Variation in oviposition patterns could be a response to variation in host plant defenses. 5. In nature, weevils strictly oviposited on their respective host plants, while in bioassays, R. lineaticollis exhibited strong preference for A. syriaca and R. annectens fed equally on both host plants. 6. Overall, our results support that milkweed stem weevils are strict specialists but might be undergoing changes in host use. R. lineaticollis specializes on A. syriaca but has two distinct modes of oviposition. Meanwhile R. annectens seems to be more accepting of other hosts. We hypothesize that these weevils might be shifting host use associated with changes in host plant distributions.

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Insect adaptations toward plant toxins in milkweed–herbivores systems – a review

Cited by 30 publications

References 103 publications

What doesn’t kill you makes you stronger: The burdens and benefits of toxin sequestration in a milkweed aphid

What doesn’t kill you makes you stronger: The burdens and benefits of toxin sequestration in a milkweed aphid

Phenotypic and Transcriptomic Response of the Grasshopper Oedaleus asiaticus (Orthoptera: Acrididae) to Toxic Rutin

Host specificity and variation in oviposition behaviour of milkweed stem weevils and implications for species divergence

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