Climate warming can reduce biocontrol efficacy and promote plant invasion due to both genetic and transient metabolomic changes.

Climate change may affect plant-herbivore interactions and their associated ecosystem functions. In an experimental evolution approach, we subjected replicated populations of the invasive Ambrosia artemisiifolia to a combination of simulated warming and herbivory by a potential biocontrol beetle. We tracked genomic and metabolomic changes across generations in field populations and assessed plant offspring phenotypes in a common environment. Using an integrated Bayesian model, we show that increased offspring biomass in response to warming arose through changes in the genetic composition of populations. In contrast, increased resistance to herbivory arose through a shift in plant metabolomic profiles without genetic changes, most likely by transgenerational induction of defences. Importantly, while increased resistance was costly at ambient temperatures, warming removed this constraint and favoured both vigorous and better defended plants under biocontrol. Climate warming may thus decrease biocontrol efficiency and promote Ambrosia invasion, with potentially serious economic and health consequences

Climate warming can reduce biocontrol efficacy and promote plant invasion due to both genetic and transient metabolomic changes

Climate change may affect plant-herbivore interactions and their associated ecosystem functions. In an experimental evolution approach, we subjected replicated populations of the invasive Ambrosia artemisiifolia to a combination of simulated warming and herbivory by a potential biocontrol beetle. We tracked genomic and metabolomic changes across generations in field populations and assessed plant offspring phenotypes in a common environment. Using an integrated Bayesian model, we show that increased offspring biomass in response to warming arose through changes in the genetic composition of populations. In contrast, increased resistance to herbivory arose through a shift in plant metabolomic profiles without genetic changes, most likely by transgenerational induction of defences. Importantly, while increased resistance was costly at ambient temperatures, warming removed this constraint and favoured both vigorous and better defended plants under biocontrol. Climate warming may thus decrease biocontrol efficiency and promote Ambrosia invasion, with potentially serious economic and health consequences

Metabolization and sequestration of plant specialized metabolites in insect herbivores: Current and emerging approaches

Herbivorous insects encounter diverse plant specialized metabolites (PSMs) in their diet, that have deterrent, anti-nutritional, or toxic properties. Understanding how they cope with PSMs is crucial to understand their biology, population dynamics, and evolution. This review summarizes current and emerging cutting-edge methods that can be used to characterize the metabolic fate of PSMs, from ingestion to excretion or sequestration. It further emphasizes a workflow that enables not only to study PSM metabolism at different scales, but also to tackle and validate the genetic and biochemical mechanisms involved in PSM resistance by herbivores. This review thus aims at facilitating research on PSM-mediated plant-herbivore interactions

Metabolization and sequestration of plant specialized metabolites in insect herbivores: Current and emerging approaches.

Herbivorous insects encounter diverse plant specialized metabolites (PSMs) in their diet, that have deterrent, anti-nutritional, or toxic properties. Understanding how they cope with PSMs is crucial to understand their biology, population dynamics, and evolution. This review summarizes current and emerging cutting-edge methods that can be used to characterize the metabolic fate of PSMs, from ingestion to excretion or sequestration. It further emphasizes a workflow that enables not only to study PSM metabolism at different scales, but also to tackle and validate the genetic and biochemical mechanisms involved in PSM resistance by herbivores. This review thus aims at facilitating research on PSM-mediated plant-herbivore interactions

Sequestration of Defenses against Predators Drives Specialized Host Plant Associations in Preadapted Milkweed Bugs (Heteroptera: Lygaeinae)

AbstractHost plant specialization across herbivorous insects varies dramatically, but while the molecular mechanisms of host plant adaptations are increasingly known, we often lack a comprehensive understanding of the selective forces that favor specialization. The milkweed bugs (Heteroptera: Lygaeinae) are ancestrally associated with plants of the Apocynaceae from which they commonly sequester cardiac glycosides for defense, facilitated by resistant NaNa+/K+-ATPases and adaptations for transport, storage, and discharge of toxins. Here, we show that three Lygaeinae species independently colonized four novel nonapocynaceous hosts that convergently produce cardiac glycosides. A fourth species shifted to a new source of toxins by tolerating and sequestering alkaloids from meadow saffron (Colchicum autumnale, Colchicaceae). Across three milkweed bug species tested, feeding on seeds containing toxins did not improve growth or speed of development and even impaired growth and development in two species, but sequestration mediated protection of milkweed bugs against two natural predators: lacewing larvae and passerine birds. We conclude that physiological preadaptations and convergent phytochemistry facilitated novel specialized host associations. Since toxic seeds did not improve growth but either impaired growth or, at most, had neutral effects, selection by predators on sequestration of defenses, rather than the exploitation of additional profitable dietary resources, can lead to obligatory specialized host associations in otherwise generalist insects

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

Phytochemical diversity is thought to result from coevolutionary cycles as specialization in herbivores imposes diversifying selection on plant chemical defenses. Plants in the speciose genus Erysimum (Brassicaceae) produce both ancestral glucosinolates and evolutionarily novel cardenolides as defenses. Here we test macroevolutionary hypotheses on co-expression, co-regulation, and diversification of these potentially redundant defenses across this genus. We sequenced and assembled the genome of E. cheiranthoides and foliar transcriptomes of 47 additional Erysimum species to construct a phylogeny from 9868 orthologous genes, revealing several geographic clades but also high levels of gene discordance. Concentrations, inducibility, and diversity of the two defenses varied independently among species, with no evidence for trade-offs. Closely related, geographically co-occurring species shared similar cardenolide traits, but not glucosinolate traits, likely as a result of specific selective pressures acting on each defense. Ancestral and novel chemical defenses in Erysimum thus appear to provide complementary rather than redundant functions.Austrian Science Fund (FWF) PZ00P3-161472National Science Foundation (NSF) 1811965 1645256Triad FoundationGerman Research Foundation (DFG) DFG-PE 2059/3-1Agencia Estatal de Investigacion CGL2017-86626-C2-2-PLOEWE Program Insect Biotechnology and BioresourcesJunta de Andalucía A-RNM505-UGR1

Chemistry data

Tab-delimited file containing chemistry data of plant (Sample.type = Pl), aphid (Sample.type = Aph), and honeydew (Sample.type = Hd) samples. 'Chamber' refers to one of two growth chambers. For a subset of plant samples, the foliar C:N ratio is given in column 'C.N'. All columns headed with cX.X are individual cardenolide compounds [ng/mg sample], with X.X referring to their HPLC retention time

Plant chemical defense indirectly mediates aphid performance via interactions with tending ants

The benefits of mutualistic interactions are often highly context dependent. We studied the interaction between the milkweed aphid Aphis asclepiadis and a tending ant, Formica podzolica. While this interaction is generally considered beneficial, variation in plant genotype may alter it from mutualistic to antagonistic. Here we link the shift in strength and relative benefit of the ant-aphid interaction to plant genotypic variation in the production of cardenolides, a class of toxic defensive chemicals. In a field experiment with highly variable genotypes of the common milkweed (Asclepias syriaca), we show that plant cardenolides, especially polar forms, are ingested and excreted by the aphid proportionally to plant concentrations without directly affecting aphid performance. Ants consume honeydew, and aphids that excreted high amounts of cardenolides received fewer ant visits, in turn reducing aphid survival. On at least some plant genotypes, aphid numbers per plant were reduced in the presence of ants to levels lower than in corresponding ant-exclusion treatments, suggesting antagonistic ant behavior. While cardenolides thus appear ineffective as direct plant defenses against aphids, the multi-trophic context reveals an ant-mediated negative indirect effect on aphid performance and population dynamics

Trade-offs between plant growth and defense against insect herbivory: an emerging mechanistic synthesis

Costs of defense are central to our understanding of interactions between organisms and their environment, and defensive phenotypes of plants have long been considered to be constrained by trade-offs that reflect the allocation of limiting resources. Recent advances in uncovering signal transduction networks have revealed that defense trade-offs often are the result of regulatory “decisions” by the plant, enabling it to fine-tune its phenotype in response to diverse environmental challenges. We place these results in the context of classic studies in ecology and evolutionary biology, and propose a unifying framework for growth-defense trade-offs as a means to study the plant’s allocation of limiting resources. Pervasive physiological costs constrain the upper limit to growth and defense traits, but the diversity of selective pressures on plants often favors negative correlations at intermediate trait levels. Despite the ubiquity of underlying costs of defense, the current challenge is using physiological and molecular approaches to predict the conditions where they manifest as detectable trade-offs