Leaffooted Bugs: Insect Pest Species of Growing Concern for Agriculture.

Leptoglossus (Hemiptera: Coreidae) are a diverse genus of phytophagous insects. Literature regarding Leptoglossus has increased as species are identified as emerging agricultural pests or reported outside of their native range. Within Leptoglossus, five species dominate the literature and are known pests and vectors of plant pathogenic microbes in several major crops. Despite the increasing profile of Leptoglossus, current monitoring and management methods rely primarily on visual inspection, and semiochemical tools have yet to be developed. This Perspective identifies and discusses gaps in the Leptoglossus literature as well as areas of research needed for the development of effective tools for monitoring insect populations and enabling informed pest-management practices.

Maize terpene synthase 1 impacts insect behavior via the production of monoterpene volatiles ß-myrcene and linalool.

Plant-derived volatiles are important mediators of plant-insect interactions as they can provide cues for host location and quality, or act as direct or indirect defense molecules. The volatiles produced by Zea mays (maize) include a range of terpenes, likely produced by several of the terpene synthases (TPS) present in maize. Determining the roles of specific terpene volatiles and individual TPSs in maize-insect interactions is challenging due to the promiscuous nature of TPSs in vitro and their potential for functional redundancy. In this study, we used metabolite GWAS of a sweetcorn diversity panel infested with Spodoptera frugiperda (fall armyworm) to identify genetic correlations between TPSs and individual volatiles. This analysis revealed a correlation between maize terpene synthase 1 (ZmTPS1) and emission of the monoterpene volatiles linalool and ß-myrcene. Electroantennogram assays showed gravid S. frugiperda could detect both linalool and ß-myrcene. Quantification of headspace volatiles in a maize tps1 loss-of-function mutant confirmed that ZmTPS1 is an important contributor to linalool and ß-myrcene emission in maize. Furthermore, pairwise choice assays between tps1 mutant and wild-type plants showed that ZmTPS1, and by extension its volatile products, aid host location in the chewing insect S. frugiperda, yet repel the sap-sucking pest, Rhopalosiphum maidis (corn leaf aphid). On the other hand, ZmTPS1 had no impact on indirect defense via the recruitment of the parasitoid Cotesia marginiventris. ZmTPS1 is therefore an important mediator of the interactions between maize and its insect pests.

Early infestation volatile biomarkers of fruit fly Bactrocera dorsalis (Hendel) ovipositional activity in mango (Mangifera indica L.).

Infestation of agricultural commodities by insect pests results in significant economic, import and export, food safety, and invasive insect introduction issues for growers, consumers, and inspectors. The Oriental fruit fly (Bactrocera dorsalis) is considered a highly invasive insect pest with populations reported in more than 60 countries, with prevalent distributions in Asia and Africa. B. dorsalis is phytophagous with a host range encompassing hundreds of fruits and vegetables. Damage to the fruit or vegetable is inflicted through oviposition and subsequent larval feeding resulting in spoilage. Early detection of insect pest infestations is a critical component for ensuring food safety as well as controlling introduction and spread of invasive insects. However, detection of ovipositional activity and early larval development is visually difficult, thus rapid and non-destructive detection often relies on odors associated with infestation. We investigated the odors of mangoes (Mangifera indica L.) infested with B. dorsalis and compared the volatile profiles of infested mangoes to non-infested and mechanically damaged mangoes 24 h post-infestation. GC-MS and multivariate analyses provided the identification of eleven compounds unique to infested mangoes compared to mechanically damaged or non-infested fruit. Results indicated compositional and quantitative differentiation of volatile profiles among treatments for detection of infested fruit at quality checks or points of commerce.

Genetic and spatial variation in vegetative and floral traits across a hybrid zone.

PREMISE: Genetic variation influences the potential for evolution to rescue populations from impacts of environmental change. Most studies of genetic variation in fitness-related traits focus on either vegetative or floral traits, with few on floral scent. How vegetative and floral traits compare in potential for adaptive evolution is poorly understood. METHODS: We measured variation across source populations, planting sites, and genetic families for vegetative and floral traits in a hybrid zone. Seeds from families of Ipomopsis aggregata, I. tenuituba, and F1 and F2 hybrids of the two species were planted into three common gardens. Measured traits included specific leaf area (SLA), trichomes, water-use efficiency (WUE), floral morphology, petal color, nectar, and floral volatiles. RESULTS: Vegetative traits SLA and WUE varied greatly among planting sites, while showing weak or no genetic variation among source populations. Specific leaf area and trichomes responded plastically to snowmelt date, and SLA exhibited within-population genetic variation. All aspects of floral morphology varied genetically among source populations, and corolla length, corolla width, and sepal width varied genetically within populations. Heritability was not detected for volatiles due to high environmental variation, although one terpene had high evolvability, and high emission of two terpenes, a class of compounds emitted more strongly from the calyx than the corolla, correlated genetically with sepal width. Environmental variation across sites was weak for floral morphology and stronger for volatiles and vegetative traits. The inheritance of three of four volatiles departed from additive. CONCLUSIONS: Results indicate stronger genetic potential for evolutionary responses to selection in floral morphology compared with scent and vegetative traits and suggest potentially adaptive plasticity in some vegetative traits.

Evolution of selfing syndrome and its influence on genetic diversity and inbreeding: A range-wide study in Oenothera primiveris.

PREMISE: To avoid inbreeding depression, plants have evolved diverse breeding systems to favor outcrossing, such as self-incompatibility. However, changes in biotic and abiotic conditions can result in selective pressures that lead to a breakdown in self-incompatibility. The shift to increased selfing is commonly associated with reduced floral features, lower attractiveness to pollinators, and increased inbreeding. We tested the hypothesis that the loss of self-incompatibility, a shift to self-fertilization (autogamy), and concomitant evolution of the selfing syndrome (reduction in floral traits associated with cross-fertilization) will lead to increased inbreeding and population differentiation in Oenothera primiveris. Across its range, this species exhibits a shift in its breeding system and floral traits from a self-incompatible population with large flowers to self-compatible populations with smaller flowers. METHODS: We conducted a breeding system assessment, evaluated floral traits in the field and under controlled conditions, and measured population genetic parameters using RADseq data. RESULTS: Our results reveal a bimodal transition to the selfing syndrome from the west to the east of the range of O. primiveris. This shift includes variation in the breeding system and the mating system, a reduction in floral traits (flower diameter, herkogamy, and scent production), a shift to greater autogamy, reduced genetic diversity, and increased inbreeding. CONCLUSIONS: The observed variation highlights the importance of range-wide studies to understand breeding system variation and the evolution of the selfing syndrome within populations and species.

Mutualism has its limits: consequences of asymmetric interactions between a well-defended plant and its herbivorous pollinator.

Concern for pollinator health often focuses on social bees and their agricultural importance at the expense of other pollinators and their ecosystem services. When pollinating herbivores use the same plants as nectar sources and larval hosts, ecological conflicts emerge for both parties, as the pollinator's services are mitigated by herbivory and its larvae are harmed by plant defences. We tracked individual-level metrics of pollinator health-growth, survivorship, fecundity-across the life cycle of a pollinating herbivore, the common hawkmoth, Hyles lineata, interacting with a rare plant, Oenothera harringtonii, that is polymorphic for the common floral volatile (R)-(-)-linalool. Linalool had no impact on floral attraction, but its experimental addition suppressed oviposition on plants lacking linalool. Plants showed robust resistance against herbivory from leaf-disc to whole-plant scales, through poor larval growth and survivorship. Higher larval performance on other Oenothera species indicates that constitutive herbivore resistance by O. harringtonii is not a genus-wide trait. Leaf volatiles differed among populations of O. harringtonii but were not induced by larval herbivory. Similarly, elagitannins and other phenolics varied among plant tissues but were not herbivore-induced. Our findings highlight asymmetric plant-pollinator interactions and the importance of third parties, including alternative larval host plants, in maintaining pollinator health. This article is part of the theme issue 'Natural processes influencing pollinator health: from chemistry to landscapes'.

Differential gene expression associated with a floral scent polymorphism in the evening primrose Oenothera harringtonii (Onagraceae).

BACKGROUND: Plant volatiles play an important role in both plant-pollinator and plant-herbivore interactions. Intraspecific polymorphisms in volatile production are ubiquitous, but studies that explore underlying differential gene expression are rare. Oenothera harringtonii populations are polymorphic in floral emission of the monoterpene (R)-(-)-linalool; some plants emit (R)-(-)-linalool (linalool+ plants) while others do not (linalool- plants). However, the genes associated with differential production of this floral volatile in Oenothera are unknown. We used RNA-Seq to broadly characterize differential gene expression involved in (R)-(-)-linalool biosynthesis. To identify genes that may be associated with the polymorphism for this trait, we used RNA-Seq to compare gene expression in six different Oenothera harringtonii tissues from each of three linalool+ and linalool- plants. RESULTS: Three clusters of differentially expressed genes were enriched for terpene synthase activity: two were characterized by tissue-specific upregulation and one by upregulation only in plants with flowers that produce (R)-(-)-linalool. A molecular phylogeny of all terpene synthases identified two putative (R)-(-)-linalool synthase transcripts in Oenothera harringtonii, a single allele of which is found exclusively in linalool+ plants. CONCLUSIONS: By using a naturally occurring polymorphism and comparing different tissues, we were able to identify candidate genes putatively involved in the biosynthesis of (R)-(-)-linalool. Expression of these genes in linalool- plants, while low, suggests a regulatory polymorphism, rather than a population-specific loss-of-function allele. Additional terpene biosynthesis-related genes that are up-regulated in plants that emit (R)-(-)-linalool may be associated with herbivore defense, suggesting a potential economy of scale between plant reproduction and defense.

Associative learning of non-sugar nectar components: amino acids modify nectar preference in a hawkmoth.

The nearly ubiquitous presence of amino acids in the nectar of flowering plants has led to significant interest in the relevance of these compounds to pollinator behavior and physiology. A number of flower-visiting animals exhibit behavioral preferences for nectar solutions containing amino acids, but these preferences vary by species and are often context or condition dependent. Furthermore, the relative strength of these preferences and potential influence on the foraging behavior of flower-visiting animals remains unclear. Here, we used innate preference tests and associative learning paradigms to examine the nectar preferences of the flower-visiting hawkmoth Manduca sexta, in relation to both sugar and amino acid content. Manduca sexta exhibited a strong preference for higher sucrose concentrations, while the effect of amino acids on innate feeding preference was only marginally significant. However, with experience, moths were able to learn nectar composition and flower color associations and to forage preferentially (against innate color preference) for nectar with a realistic amino acid composition. Foraging moths responding to learned color cues of nectar amino acid content exhibited a behavioral preference comparable to that observed in response to a 5% difference in nectar sucrose concentration. These results demonstrate that experienced foragers may assess nectar amino acid content in addition to nectar sugar content and caloric value during nectar-foraging bouts.

Diel rhythms and sex differences in the locomotor activity of hawkmoths.

Circadian patterns of activity are considered ubiquitous and adaptive, and are often invoked as a mechanism for temporal niche partitioning. Yet, comparisons of rhythmic behavior in related animal species are uncommon. This is particularly true of Lepidoptera (butterflies and moths), in which studies of whole-animal patterns of behavior are far outweighed by examinations of tissue-specific molecular clocks. Here, we used a comparative approach to examine the circadian patterns of flight behavior in Manduca sexta and Hyles lineata [two distantly related species of hawkmoth (Sphingidae)]. By filming isolated, individual animals, we were able to examine rhythmic locomotor (flight) activity at the species level, as well as at the level of the individual sexes, and in the absence of interference from social interaction. Our results confirmed classic descriptions of strictly nocturnal behavior in M. sexta and demonstrated a dramatically different activity pattern in H. lineata Furthermore, we showed distinct species and sex-specific differences in the maintenance of the endogenous rhythm under conditions of constant darkness. In both species, female activity peaked in advance of males whereas male activity coincided with periods of female sexual receptivity. This suggests a role for circadian patterns of locomotor activity in synchronizing periods of sexual receptivity between the sexes.

Olfaction in context-sources of nuance in plant-pollinator communication.

Floral scents act as long-distance signals to attract pollinators, but volatiles emitted from the vegetation and neighboring plant community may modify this mutualistic communication system. What impact does the olfactory background have on pollination systems and their evolution? We consider recent behavioral studies that address the context of when and where volatile backgrounds influence a pollinator's perception of floral blends. In parallel, we review neurophysiological studies that show the importance of blend composition and background in modifying the representation of floral blends in the pollinator brain, as well as experience-dependent plasticity in increasing the representation of a rewarding odor. Here, we suggest that the efficacy of the floral blend in different environments may be an important selective force shaping differences in pollinator olfactory receptor expression and underlying neural mechanisms that mediate flower visitation and plant reproductive isolation.

Diminished MTORC1-Dependent JNK Activation Underlies the Neurodevelopmental Defects Associated with Lysosomal Dysfunction.

Here, we evaluate the mechanisms underlying the neurodevelopmental deficits in Drosophila and mouse models of lysosomal storage diseases (LSDs). We find that lysosomes promote the growth of neuromuscular junctions (NMJs) via Rag GTPases and mechanistic target of rapamycin complex 1 (MTORC1). However, rather than employing S6K/4E-BP1, MTORC1 stimulates NMJ growth via JNK, a determinant of axonal growth in Drosophila and mammals. This role of lysosomal function in regulating JNK phosphorylation is conserved in mammals. Despite requiring the amino-acid-responsive kinase MTORC1, NMJ development is insensitive to dietary protein. We attribute this paradox to anaplastic lymphoma kinase (ALK), which restricts neuronal amino acid uptake, and the administration of an ALK inhibitor couples NMJ development to dietary protein. Our findings provide an explanation for the neurodevelopmental deficits in LSDs and suggest an actionable target for treatment.

A TRPV channel in Drosophila motor neurons regulates presynaptic resting Ca2+ levels, synapse growth, and synaptic transmission.

Presynaptic resting Ca(2+) influences synaptic vesicle (SV) release probability. Here, we report that a TRPV channel, Inactive (Iav), maintains presynaptic resting [Ca(2+)] by promoting Ca(2+) release from the endoplasmic reticulum in Drosophila motor neurons, and is required for both synapse development and neurotransmission. We find that Iav activates the Ca(2+)/calmodulin-dependent protein phosphatase calcineurin, which is essential for presynaptic microtubule stabilization at the neuromuscular junction. Thus, loss of Iav induces destabilization of presynaptic microtubules, resulting in diminished synaptic growth. Interestingly, expression of human TRPV1 in Iav-deficient motor neurons rescues these defects. We also show that the absence of Iav causes lower SV release probability and diminished synaptic transmission, whereas Iav overexpression elevates these synaptic parameters. Together, our findings indicate that Iav acts as a key regulator of synaptic development and function by influencing presynaptic resting [Ca(2+)].