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1.
Plant J ; 119(1): 84-99, 2024 Jul.
Article in English | MEDLINE | ID: mdl-38578218

ABSTRACT

Tuta absoluta ("leafminer"), is a major pest of tomato crops worldwide. Controlling this insect is difficult due to its efficient infestation, rapid proliferation, and resilience to changing weather conditions. Furthermore, chemical pesticides have only a short-term effect due to rapid development of T. absoluta strains. Here, we show that a variety of tomato cultivars, treated with external phenylalanine solutions exhibit high resistance to T. absoluta, under both greenhouse and open field conditions, at different locations. A large-scale metabolomic study revealed that tomato leaves absorb and metabolize externally given Phe efficiently, resulting in a change in their volatile profile, and repellence of T. absoluta moths. The change in the volatile profile is due to an increase in three phenylalanine-derived benzenoid phenylpropanoid volatiles (BPVs), benzaldehyde, phenylacetaldehyde, and 2-phenylethanol. This treatment had no effect on terpenes and green leaf volatiles, known to contribute to the fight against insects. Phe-treated plants also increased the resistance of neighboring non-treated plants. RNAseq analysis of the neighboring non-treated plants revealed an exclusive upregulation of genes, with enrichment of genes related to the plant immune response system. Exposure of tomato plants to either benzaldehyde, phenylacetaldehyde, or 2-phenylethanol, resulted in induction of genes related to the plant immune system that were also induced due to neighboring Phe-treated plants. We suggest a novel role of phenylalanine-derived BPVs as mediators of plant-insect interactions, acting as inducers of the plant defense mechanisms.


Subject(s)
Phenylalanine , Plant Leaves , Solanum lycopersicum , Volatile Organic Compounds , Solanum lycopersicum/genetics , Solanum lycopersicum/metabolism , Solanum lycopersicum/parasitology , Phenylalanine/metabolism , Volatile Organic Compounds/metabolism , Animals , Plant Leaves/metabolism , Plant Leaves/drug effects , Plant Leaves/parasitology , Benzaldehydes/metabolism , Benzaldehydes/pharmacology , Acetaldehyde/analogs & derivatives , Acetaldehyde/metabolism , Acetaldehyde/pharmacology , Moths/physiology , Moths/drug effects , Plant Diseases/parasitology , Plant Diseases/immunology , Manduca/physiology
2.
Proc Natl Acad Sci U S A ; 119(42): e2202852119, 2022 10 18.
Article in English | MEDLINE | ID: mdl-36215482

ABSTRACT

Fossilized leaves provide the longest running record of hyperdiverse plant-insect herbivore associations. Reconstructions of these relationships over deep time indicate strong links between environmental conditions, herbivore diversity, and feeding damage on leaves. However, herbivory has not been compared between the past and the modern era, which is characterized by intense anthropogenic environmental change. Here, we present estimates for damage frequencies and diversities on fossil leaves from the Late Cretaceous (66.8 Ma) through the Pleistocene (2.06 Ma) and compare these estimates with Recent (post-1955) leaves collected via paleobotanical methods from modern ecosystems: Harvard Forest, United States; the Smithsonian Environmental Research Center, United States; and La Selva, Costa Rica. Total damage frequency, measured as the percentage of leaves with any herbivore damage, within modern ecosystems is greater than any fossil locality within this record. This pattern is driven by increased frequencies across nearly all functional feeding groups within the Recent. Diversities of total, specialized, and mining damage types are elevated within the Recent compared with fossil floras. Our results demonstrate that plants in the modern era are experiencing unprecedented levels of insect damage, despite widespread insect declines. Human influence, such as the rate of global climate warming, influencing insect feeding and timing of life cycle processes along with urbanization and the introduction of invasive plant and insect species may drive elevated herbivory. This research suggests that the strength of human influence on plant-insect interactions is not controlled by climate change alone but rather, the way in which humans interact with terrestrial landscape.


Subject(s)
Fossils , Herbivory , Animals , Ecosystem , Forests , Humans , Insecta , Plant Leaves , Plants
3.
Proc Natl Acad Sci U S A ; 119(25): e2205073119, 2022 06 21.
Article in English | MEDLINE | ID: mdl-35696564

ABSTRACT

Environmental clines in organismal defensive traits are usually attributed to stronger selection by enemies at lower latitudes or near the host's range center. Nonetheless, little functional evidence has supported this hypothesis, especially for coevolving plants and herbivores. We quantified cardenolide toxins in seeds of 24 populations of common milkweed (Asclepias syriaca) across 13 degrees of latitude, revealing a pattern of increasing cardenolide concentrations toward the host's range center. The unusual nitrogen-containing cardenolide labriformin was an exception and peaked at higher latitudes. Milkweed seeds are eaten by specialist lygaeid bugs that are even more tolerant of cardenolides than the monarch butterfly, concentrating most cardenolides (but not labriformin) from seeds into their bodies. Accordingly, whether cardenolides defend seeds against these specialist bugs is unclear. We demonstrate that Oncopeltus fasciatus (Lygaeidae) metabolized two major compounds (glycosylated aspecioside and labriformin) into distinct products that were sequestered without impairing growth. We next tested several isolated cardenolides in vitro on the physiological target of cardenolides (Na+/K+-ATPase); there was little variation among compounds in inhibition of an unadapted Na+/K+-ATPase, but tremendous variation in impacts on that of monarchs and Oncopeltus. Labriformin was the most inhibitive compound tested for both insects, but Oncopeltus had the greater advantage over monarchs in tolerating labriformin compared to other compounds. Three metabolized (and stored) cardenolides were less toxic than their parent compounds found in seeds. Our results suggest that a potent plant defense is evolving by natural selection along a geographical cline and targets specialist herbivores, but is met by insect tolerance, detoxification, and sequestration.


Subject(s)
Asclepias , Butterflies , Cardenolides , Heteroptera , Plant Defense Against Herbivory , Adenosine Triphosphatases/metabolism , Animals , Asclepias/metabolism , Butterflies/metabolism , Cardenolides/chemistry , Cardenolides/metabolism , Cardenolides/toxicity , Herbivory , Heteroptera/metabolism , Seeds/metabolism
4.
Proc Natl Acad Sci U S A ; 119(51): e2208447119, 2022 12 20.
Article in English | MEDLINE | ID: mdl-36508662

ABSTRACT

Coevolutionary interactions are responsible for much of the Earth's biodiversity, with key innovations driving speciation bursts on both sides of the interaction. One persistent question is whether macroevolutionary traits identified as key innovations accurately predict functional performance and selection dynamics within species, as this necessitates characterizing their function, investigating their fitness consequences, and exploring the selection dynamics acting upon them. Here, we used CRISPR-Cas9 mediating nonhomologous end joining (NHEJ) in the butterfly species Pieris brassicae to knock out and directly assess the function and fitness impacts of nitrile specifier protein (NSP) and major allergen (MA). These are two closely related genes that facilitate glucosinolate (GSL) detoxification capacity, which is a key innovation in mustard feeding Pierinae butterflies. We find NSP and MA are both required for survival on plants containing GSLs, with expression differences arising in response to variable GSL profiles, concordant with detoxification performance. Importantly, this concordance was only observed when using natural host plants, likely reflecting the complexity of how these enzymes interact with natural plant variation in GSLs and myrosinases. Finally, signatures of positive selection for NSP and MA were detected across Pieris species, consistent with these genes' importance in recent coevolutionary interactions. Thus, the war between these butterflies and their host plants involves more than the mere presence of chemical defenses and detoxification mechanisms, as their regulation and activation represent key components of complex interactions. We find that inclusion of these dynamics, in ecologically relevant assays, is necessary for coevolutionary insights in this system and likely others.


Subject(s)
Butterflies , Animals , Butterflies/physiology , Mustard Plant/genetics , Mustard Plant/metabolism , Glucosinolates/metabolism , Plant Oils
5.
Annu Rev Entomol ; 69: 277-302, 2024 Jan 25.
Article in English | MEDLINE | ID: mdl-37738463

ABSTRACT

Psyllids constitute a diverse group of sap-feeding Sternorrhyncha that were relatively obscure until it was discovered that a handful of species transmit bacterial plant pathogens. Yet the superfamily Psylloidea is much richer than the sum of its crop-associated vectors, with over 4,000 described species exhibiting diverse life histories and host exploitation strategies. A growing body of research is uncovering fascinating insights into psyllid evolution, biology, behavior, and species interactions. This work has revealed commonalities and differences with better-studied Sternorrhyncha, as well as unique evolutionary patterns of lineage divergence and host use. We are also learning how psyllid evolution and foraging ecology underlie life history traits and the roles of psyllids in communities. At finer scales, we are untangling the web of symbionts across the psyllid family tree, linking symbiont and psyllid lineages, and revealing mechanisms underlying reciprocal exchange between symbiont and host. In this review, we synthesize and summarize key advances within these areas with a focus on free-living (nongalling) Psylloidea.


Subject(s)
Hemiptera , Life History Traits , Animals , Hemiptera/microbiology , Phylogeny , Bacteria , Biology
6.
Annu Rev Entomol ; 69: 527-550, 2024 Jan 25.
Article in English | MEDLINE | ID: mdl-38270985

ABSTRACT

Locusts are grasshoppers that can migrate en masse and devastate food security. Plant nutrient content is a key variable influencing population dynamics, but the relationship is not straightforward. For an herbivore, plant quality depends not only on the balance of nutrients and antinutrients in plant tissues, which is influenced by land use and climate change, but also on the nutritional state and demands of the herbivore, as well as its capacity to extract nutrients from host plants. In contrast to the concept of a positive relationship between nitrogen or protein concentration and herbivore performance, a five-decade review of lab and field studies indicates that equating plant N to plant quality is misleading because grasshoppers respond negatively or neutrally to increasing plant N just as often as they respond positively. For locusts specifically, low-N environments are actually beneficial because they supply high energy rates that support migration. Therefore, intensive land use, such as continuous grazing or cropping, and elevated ambient CO2 levels that decrease the protein:carbohydrate ratios of plants are predicted to broadly promote locust outbreaks.


Subject(s)
Grasshoppers , Animals , Ecosystem , Plants , Herbivory , Nutrients
7.
Plant J ; 114(5): 1164-1177, 2023 06.
Article in English | MEDLINE | ID: mdl-36891808

ABSTRACT

Non-volatile metabolites constitute the bulk of plant biomass. From the perspective of plant-insect interactions, these structurally diverse compounds include nutritious core metabolites and defensive specialized metabolites. In this review, we synthesize the current literature on multiple scales of plant-insect interactions mediated by non-volatile metabolites. At the molecular level, functional genetics studies have revealed a large collection of receptors targeting plant non-volatile metabolites in model insect species and agricultural pests. By contrast, examples of plant receptors of insect-derived molecules remain sparse. For insect herbivores, plant non-volatile metabolites function beyond the dichotomy of core metabolites, classed as nutrients, and specialized metabolites, classed as defensive compounds. Insect feeding tends to elicit evolutionarily conserved changes in plant specialized metabolism, whereas its effect on plant core metabolism varies widely based the interacting species. Finally, several recent studies have demonstrated that non-volatile metabolites can mediate tripartite communication on the community scale, facilitated by physical connections established through direct root-to-root communication, parasitic plants, arbuscular mycorrhizae and the rhizosphere microbiome. Recent advances in both plant and insect molecular biology will facilitate further research on the role of non-volatile metabolites in mediating plant-insect interactions.


Subject(s)
Herbivory , Mycorrhizae , Animals , Herbivory/physiology , Insecta/physiology , Plants/metabolism , Rhizosphere
8.
Ecol Lett ; 27(9): e14499, 2024 Sep.
Article in English | MEDLINE | ID: mdl-39354894

ABSTRACT

Shelter-building insects are important ecosystem engineers, playing critical roles in structuring arthropod communities. Nonetheless, the influence of leaf shelters and arthropods on plant-associated microbiota remains largely unexplored. Arthropods that visit or inhabit plants can contribute to the leaf microbial community, resulting in significant changes in plant-microbe interactions. By artificially constructing leaf shelters, we provide evidence that shelter-building insects influence not only the arthropod community structure but also impact the phyllosphere microbiota. Leaf shelters exhibited higher abundance and richness of arthropods, changing the associated arthropod community composition. These shelters also altered the composition and community structure of phyllosphere microbiota, promoting greater richness and diversity of bacteria at the phyllosphere. In leaf shelters, microbial diversity positively correlated with the richness and diversity of herbivores. These findings demonstrate the critical role of leaf shelters in structuring both arthropod and microbial communities through altered microhabitats and species interactions.


Subject(s)
Arthropods , Biodiversity , Microbiota , Plant Leaves , Animals , Plant Leaves/microbiology , Arthropods/microbiology , Bacteria/classification , Bacteria/genetics , Ecosystem , Herbivory
9.
Am Nat ; 204(4): 416-431, 2024 Oct.
Article in English | MEDLINE | ID: mdl-39326060

ABSTRACT

AbstractThe influence of climate on deep-time plant-insect interactions is becoming increasingly well known, with temperature, CO2 increases (and associated stoichiometric changes in plants), and aridity likely playing a critical role. In our modern climate, all three factors are shifting at an unprecedented rate, with uncertain consequences for biodiversity. To investigate effects of temperature, stoichiometry (specifically that of nitrogen), and aridity on insect herbivory, we explored insect herbivory in three modern floral assemblages and in 39 fossil floras, especially focusing on eight floras around a past hyperthermal event (the Paleocene-Eocene Thermal Maximum) from Bighorn Basin (BB). We find that higher temperatures were associated with increased herbivory in the past, especially among BB sites. In these BB sites, non-N2-fixing plants experienced a lower richness but higher frequency of herbivory damage than N2-fixing plants. Herbivory frequency but not richness was greater in BB sites compared with contemporaneous, nearby, but less arid sites from Hanna Basin. Compared with deep-time environments, herbivory frequency and richness are higher in modern sites, suggesting that current accelerated warming uniquely impacts plant-insect interactions. Overall, our work addresses multiple aspects of climate change using fossil data while also contextualizing the impact of modern anthropogenic change on Earth's most diverse interactions.


Subject(s)
Climate Change , Fossils , Herbivory , Insecta , Temperature , Animals , Insecta/physiology , Nitrogen/metabolism , Plants , Biodiversity
10.
Planta ; 259(5): 105, 2024 Mar 29.
Article in English | MEDLINE | ID: mdl-38551685

ABSTRACT

MAIN CONCLUSION: Monoterpenes and phenolics play distinct roles in defending white spruce trees from insect defoliators. Monoterpenes contribute to the toxicity of the foliage, deterring herbivory, whereas phenolics impede budworm growth. This study demonstrates the complex interplay between monoterpenes and phenolics and their collective influence on the defense strategy of white spruce trees against a common insect defoliator. Long-lived coniferous trees display considerable variations in their defensive chemistry. The impact of these defense phenotype variations on insect herbivores of the same species remains to be thoroughly studied, mainly due to challenges in replicating the comprehensive defense profiles of trees under controlled conditions. This study methodically examined the defensive properties of foliar monoterpenes and phenolics across 80 distinct white spruce families. These families were subsequently grouped into two chemotypes based on their foliar monoterpene concentrations. To understand the separate and combined effects of these classes on tree defenses to the eastern spruce budworm, we conducted feeding experiments using actual defense profiles from representative families. Specifically, we assessed budworm response when exposed to substrates amended with phenolics alone or monoterpenes. Our findings indicate that the ratios and amounts of monoterpenes and phenolics present in the white spruce foliage influence the survival of spruce budworms. Phenotypes associated with complete larval mortality exhibited elevated ratios (ranging from 0.4 to 0.6) and concentrations (ranging from 1143 to 1796 ng mg-1) of monoterpenes. Conversely, families characterized by higher phenolic ratios (ranging from 0.62 to 0.77) and lower monoterpene concentrations (ranging from 419 to 985 ng mg-1) were less lethal to the spruce budworm. Both classes of defense compounds contribute significantly to the overall defensive capabilities of white spruce trees. Monoterpenes appear critical in determining the general toxicity of foliage, while phenolics play a role in slowing budworm development, thereby underscoring their collective importance in white spruce defenses.


Subject(s)
Moths , Picea , Animals , Picea/genetics , Moths/physiology , Larva/physiology , Monoterpenes , Trees , Phenols
11.
New Phytol ; 242(3): 1307-1323, 2024 May.
Article in English | MEDLINE | ID: mdl-38488269

ABSTRACT

Community genetics seeks to understand the mechanisms by which natural genetic variation in heritable host phenotypes can encompass assemblages of organisms such as bacteria, fungi, and many animals including arthropods. Prior studies that focused on plant genotypes have been unable to identify genes controlling community composition, a necessary step to predict ecosystem structure and function as underlying genes shift within plant populations. We surveyed arthropods within an association population of Populus trichocarpa in three common gardens to discover plant genes that contributed to arthropod community composition. We analyzed our surveys with traditional single-trait genome-wide association analysis (GWAS), multitrait GWAS, and functional networks built from a diverse set of plant phenotypes. Plant genotype was influential in structuring arthropod community composition among several garden sites. Candidate genes important for higher level organization of arthropod communities had broadly applicable functions, such as terpenoid biosynthesis and production of dsRNA binding proteins and protein kinases, which may be capable of targeting multiple arthropod species. We have demonstrated the ability to detect, in an uncontrolled environment, individual genes that are associated with the community assemblage of arthropods on a host plant, further enhancing our understanding of genetic mechanisms that impact ecosystem structure.


Subject(s)
Arthropods , Populus , Animals , Arthropods/genetics , Ecosystem , Populus/genetics , Genome-Wide Association Study , Genotype , Genetic Variation
12.
Plant Cell Environ ; 2024 Jul 16.
Article in English | MEDLINE | ID: mdl-39011992

ABSTRACT

Over the last decade, a large effort has been made to understand how extreme climate events disrupt species interactions. Yet, it is unclear how these events affect plants and herbivores directly, via metabolic changes, and indirectly, via their subsequent altered interaction. We exposed common milkweed (Asclepias syriaca) and monarch caterpillars (Danaus plexippus) to control (26:14°C, day:night) or heat wave (HW) conditions (36:24°C, day:night) for 4 days and then moved each organism to a new control or HW partner to disentangle the direct and indirect effects of heat exposure on each organism. We found that the HW directly benefited plants in terms of growth and defence expression (increased latex exudation and total cardenolides) and insect her'bivores through faster larval development. Conversely, indirect HW effects caused both plant latex and total cardenolides to decrease after subsequent herbivory. Nonetheless, increasing trends of more toxic cardenolides and lower leaf nutritional quality after herbivory by HW caterpillars likely led to reduced plant damage compared to controls. Our findings reveal that indirect impacts of HWs may play a greater role in shaping plant-herbivore interactions via changes in key physiological traits, providing valuable understanding of how ecological interactions may proceed in a changing world.

13.
Glob Chang Biol ; 30(1): e17044, 2024 Jan.
Article in English | MEDLINE | ID: mdl-37994481

ABSTRACT

Climate change is contributing to declines of insects through rising temperatures, altered precipitation patterns, and an increasing frequency of extreme events. The impacts of both gradual and sudden shifts in weather patterns are realized directly on insect physiology and indirectly through impacts on other trophic levels. Here, we investigated direct effects of seasonal weather on butterfly occurrences and indirect effects mediated by plant productivity using a temporally intensive butterfly monitoring dataset, in combination with high-resolution climate data and a remotely sensed indicator of plant primary productivity. Specifically, we used Bayesian hierarchical path analysis to quantify relationships between weather and weather-driven plant productivity on the occurrence of 94 butterfly species from three localities distributed across an elevational gradient. We found that snow pack exerted a strong direct positive effect on butterfly occurrence and that low snow pack was the primary driver of reductions during drought. Additionally, we found that plant primary productivity had a consistently negative effect on butterfly occurrence. These results highlight mechanisms of weather-driven declines in insect populations and the nuances of climate change effects involving snow melt, which have implications for ecological theories linking topographic complexity to ecological resilience in montane systems.


Subject(s)
Butterflies , Snow , Animals , Seasons , Butterflies/physiology , Bayes Theorem , Weather , Climate Change , Ecosystem
14.
J Anim Ecol ; 2024 Sep 22.
Article in English | MEDLINE | ID: mdl-39307977

ABSTRACT

Social interactions influence disease spread, information flow and resource allocation across species, yet heterogeneity in social interaction frequency and its fitness consequences are still poorly understood. Additionally, the role of exogenous chemicals, such as non-nutritive plant metabolites that are utilised by several animal species, in shaping social networks remains unclear. Here, we investigated how non-nutritive plant metabolites impact social interactions and the lifespan of the turnip sawfly, Athalia rosae. Adult sawflies acquire neo-clerodane diterpenoids ('clerodanoids') from non-food plants and this can serve as a defence against predation and increase mating success. We found intraspecific variation in clerodanoids in natural populations and laboratory-reared individuals. Clerodanoids could also be acquired from conspecifics that had prior access to the plant metabolites, which led to increased agonistic social interactions. Network analysis indicated increased social interactions in sawfly groups where some or all individuals had prior access to clerodanoids, while groups with no prior access had fewer interactions. The frequency of social interactions was influenced by the clerodanoid status of the focal individual and that of other conspecifics. Finally, we observed a shorter lifespan in adults with prior clerodanoid access when grouped with individuals without prior access, suggesting that social interactions to obtain clerodanoids have fitness costs. Our findings highlight the role of intraspecific variation in the acquisition of non-nutritional plant metabolites in shaping social networks. This variation influences individual fitness and social interactions, thereby shaping the individualised social niche.

15.
Am J Bot ; 111(1): e16263, 2024 Jan.
Article in English | MEDLINE | ID: mdl-38014690

ABSTRACT

PREMISE: Plant traits and insect herbivory have been highly studied within the modern record but only to a limited extent within the paleontological. Preservation influences what can be measured within the fossil record, but modern methods are also not compatible with paleobotanical methods. To remedy this knowledge gap, a comparable framework was created here using modern and paleobotanical methods, allowing for future comparisons within the fossil record. METHODS: Insect feeding damage on selected tree species at Harvard Forest, the Smithsonian Environmental Research Center, and La Selva were characterized using the damage type system prevalent within paleobotanical studies and compared with leaf traits. Linear models and random forest analyses tested the influence of leaf traits on total, specialized, gall, and mine frequency and diversity. RESULTS: Structural traits like leaf dry mass per area and palatability traits, including lignin and phosphorus concentrations, are important variables affecting gall and mine damage. The significance and strength of trait-herbivory relationships varied across forest types, which is likely driven by differences in local insect populations. CONCLUSIONS: This work addresses the persistent gap between modern and paleoecological studies focusing on the influence of leaf traits on insect herbivory. This is important as modern climate change alters our understanding of plant-insect interactions, providing a need for contextualizing these relationships within evolutionary time. The fossil record provides information on terrestrial response to past climatic events and, thus, should be implemented when considering how to preserve biodiversity under current and future global change.


Subject(s)
Ecosystem , Insecta , Animals , Insecta/physiology , Herbivory , Biodiversity , Plant Leaves/physiology
16.
Am J Bot ; 111(2): e16279, 2024 02.
Article in English | MEDLINE | ID: mdl-38290989

ABSTRACT

PREMISE: Understanding the factors that limit reproductive success is a key component of plant biology. Carnivorous plants rely on insects as both nutrient sources and pollinators, providing a unique system for studying the effects of both resource and pollen limitation on plant reproduction. METHODS: We conducted a field experiment using wild-growing Dionaea muscipula J. Ellis (Droseraceae) in which we manipulated prey and pollen in a factorial design and measured flower production, number of fruits, and number of seeds. Because understanding reproduction requires knowledge of a plant species' reproductive and pollination biology, we also examined the pollination system, per-visit pollinator effectiveness, and pollen-ovule (P/O) ratio of D. muscipula. RESULTS: Plants that received supplemental prey produced more flowers than control plants. They also had a higher overall fitness estimate (number of flowers × fruit set (total fruits/total flowers) × seeds per fruit), although this benefit was significant only when prey supplementation occurred in the previous growing season. Neither pollen supplementation nor the interaction between pollen and prey supplementation significantly affected overall plant fitness. CONCLUSIONS: This study reinforces the reliance of D. muscipula on adequate prey capture for flower, fruit, and seed production and a mobile pollen vector for reproduction, indicating the importance of considering insects as part of an effective conservation management plan for this species.


Subject(s)
Carnivorous Plant , Droseraceae , Animals , Reproduction , Pollination , Plants , Insecta , Flowers
17.
Oecologia ; 204(1): 95-105, 2024 Jan.
Article in English | MEDLINE | ID: mdl-38123786

ABSTRACT

Understanding the circumstances under which insect herbivores will adopt a novel host plant is a longstanding question in basic and applied ecology. While geographic variation in host use can arise through differences in both herbivore preference and plant characteristics, there is a tendency to attribute geographic variation in host use to regional differences in herbivore preference alone. This is especially true for herbivores specialized to one or a few plant species. We compared how geographic variation in herbivore preference and host plant origin shape regional differences in host plant use by the specialized herbivore, Euphydryas phaeton. In parts of its range, E. phaeton uses only a native host, Chelone glabra, while in others, it also uses an introduced host, Plantago lanceolata. We offered female butterflies from each region the non-native host plant sourced from both regions and compared their oviposition behavior. The non-native host was almost universally rejected by butterflies in the region where only the native plant is used. In the region where butterflies use both hosts, females accepted non-native plants from their natal region twice as often as non-native plants from the other region where they are not used. Acceptance differed substantially among individual butterflies within regions but not among plants within regions. Thus, both individual preference and regional differences in both the insect and non-native host contributed to the geographic variation in different ways. These results highlight that, in addition to herbivore preference, regional differences in perceived plant suitability may be an important driver of diet breadth.


Subject(s)
Butterflies , Animals , Female , Herbivory , Larva , Plants , Diet , Oviposition
18.
J Chem Ecol ; 2024 Aug 26.
Article in English | MEDLINE | ID: mdl-39186174

ABSTRACT

Flatheaded borers (FHB; Chrysobothris spp.), are woodboring-beetles that lay their eggs in the bark and cambium of deciduous trees in North America. Females often target stressed host-plants for oviposition. The reason why is unknown; however, stressed plants often suffer various induced phytochemical changes that may enhance larval infestation success depending on the stressor such as induced upregulation of defenses, reallocation of nutrients, and changes to volatile organic compound (VOC) emissions. To understand attraction of FHB to specific stress-induced changes, we analyzed phytochemical changes associated with stress treatments and attractiveness maple trees to FHB. Trees were stressed by: (1) chemical stress (pelargonic acid herbicide), (2) physical stress (physically removing leaves), and (3) physical stress (removing portions of bark near the root crown). After reflush of defoliated trees, bark tissues where FHB larvae feed were analyzed for nutritional changes (carbon and nitrogen), anti-nutritive changes (polyphenols and tannins) and emissions of foliar VOCs. At the end of the growing season, trees were assessed for FHB larval presence and oviposition attempts. There were more larvae and oviposition attempts on trees stressed by herbicide application. Compared to other treatments, herbicide-stressed trees had greater nitrogen and total polyphenol concentrations. Greater nitrogen may play a role in the fitness of feeding larvae, and the greater polyphenol concentration may stimulate female oviposition in the herbicide stressed trees. Females may be able to locate the herbicide-stressed trees by using volatile cues such as increases in limonene, α-farnesene, (E)-4,8-dimethyl-1,3,7-nonatriene (DMNT) and hexenyl acetate.

19.
J Chem Ecol ; 50(5-6): 237-249, 2024 Jun.
Article in English | MEDLINE | ID: mdl-38713322

ABSTRACT

The orange wheat blossom midge, Sitodiplosis mosellana (Géhin) (Diptera: Cecidomyiidae), is a significant wheat pest in the Prairie Provinces of Canada and northern regions of the USA. Wheat phenology plays a critical role in wheat midge oviposition. We hypothesized that S. mosellana oviposition behaviour is influenced by volatile organic compounds (VOCs) emitted by wheat at two adjacent wheat growth stages: preanthesis and postanthesis. A higher number of S. mosellana eggs laid on preanthesis than postanthesis spikes in an oviposition choice experiment using the susceptible spring wheat cultivar 'Roblin'. In preanthesis, wheat emitted higher amounts of Z-3-hexenyl acetate (Z3-06:OAc) than at the postanthesis stage. Higher amounts of methyl ketones such as 2-tridecanone, 2-pentadecanone, and 2-undecanone were emitted by wheat in the postanthesis stage and these VOCs were sensitive to S. mosellana antennae used in the Gas Chromatography-Electroantennographic Detection. Females were attracted to synthetic Z3-06:OAc but were deterred by 2-tridecanone relative to the solvent control in the vertical Y-tube olfactometer. 2-Undecanone and 2-pentadecanone did not show any attractiveness or deterrence. In a no-choice oviposition experiment, fewer eggs were laid in preanthesis wheat exposed to a synthetic VOC blend of Z3-06:OAc, 2-undecanone, 2-tridecanone, and 2-pentadecanone at the concentrations released by postanthesis spikes. This study shows that the reduction of Z3-06:OAc, in the VOC mix, and possibly the increase in 2-tridecanone, are likely responsible for the reduction in oviposition on postanthesis wheat. These results elucidate for the first time the role of specific VOCs mediating S. mosellana oviposition in preanthesis and postanthesis wheat.


Subject(s)
Diptera , Oviposition , Triticum , Volatile Organic Compounds , Animals , Triticum/chemistry , Triticum/metabolism , Triticum/parasitology , Volatile Organic Compounds/pharmacology , Volatile Organic Compounds/metabolism , Volatile Organic Compounds/chemistry , Volatile Organic Compounds/analysis , Female , Oviposition/drug effects , Diptera/physiology , Diptera/drug effects , Acetates/pharmacology , Arthropod Antennae/physiology , Arthropod Antennae/drug effects
20.
Phytopathology ; 114(9): 2182-2191, 2024 Sep.
Article in English | MEDLINE | ID: mdl-38842916

ABSTRACT

Plant defenses are conserved among closely related species, but domestication can alter host genotypes through artificial selection with potential losses in host defenses. Therefore, both domestication and host phylogenetic structure may influence plant virus infection outcomes. Here, we examined the association of phylogeny and domestication with the fitness of infected plants. We inoculated three pairs of domesticated and wild/noncultivated squash (Cucurbita spp.) with a combination of two viruses commonly found to coinfect cucurbits, zucchini yellow mosaic virus and squash mosaic virus, and recorded fitness traits related to flowers, pollination, fruit, and seed viability in the field over 2 separate years. In an additional field experiment, we recorded the relative abundance of both viruses via RT-qPCR. We found a gradient of susceptibility across the six tested lineages, and phylogenetic structure, but not domestication, contributed to differences in infection outcomes and impacts on several fitness traits, including fruit number, fruit weight, and germination. Plant virus infection also impacted the quantity and quality of floral rewards and visitation rates of specialist bee pollinators. There were no detectable differences in viral load between the six host taxa for either virus individually or the ratio of zucchini yellow mosaic virus to squash mosaic virus. Our results highlight the importance of phylogenetic structure in predicting host susceptibility to disease across wild and domesticated plants and the ability of several hosts to maintain fitness in the field despite infection. Broader consequences of plant pathogens for beneficial insects, such as pollinators, should also be considered in future research.


Subject(s)
Cucurbita , Domestication , Phylogeny , Plant Diseases , Pollination , Potyvirus , Cucurbita/virology , Plant Diseases/virology , Potyvirus/physiology , Potyvirus/genetics , Animals , Flowers/virology , Fruit/virology , Bees/virology , Plant Viruses/physiology , Plant Viruses/genetics , Seeds/virology
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