Reproductive Dominance Strategies in Insect Social Parasites

In eusocial insects, the high cost of altruistic cooperation between colony members has favoured the evolution of cheaters that exploit social services of other species. In the most extreme forms of insect social parasitism, which has evolved multiple times across most social lineages, obligately parasitic species invade the nests of social species and manipulate the workforce of their hosts to rear their own reproductive offspring. As alien species that have lost their own sociality, these social parasites still face social challenges to infiltrate and control their hosts, thus providing independent replicates for understanding the mechanisms essential to social dominance. This review compares socially parasitic insect lineages to find general trends and build a hypothetical framework for the means by which social parasites achieve reproductive dominance. It highlights how host social organization and social parasite life history traits may impact the way they achieve reproductive supremacy, including the potential role of chemical cues. The review discusses the coevolutionary dynamics between host and parasite during this process. Altogether, this review emphasizes the value of social parasites for understanding social evolution and the need for future research in this area.     

Postgenomic chemical ecology: from genetic code to ecological interactions

Environmental response genes are defined as those encoding proteins involved in interactions external to the organism, including interactions among organisms and between the organism and its abiotic environment. The general characteristics of environmental response genes include high diversity, proliferation by duplication events, rapid rates of evolution, and tissue-or temporal-specific expression. Thus, environmental response genes include those that encode proteins involved in the manufacture, binding, transport, and breakdown of semiochemicals. Postgenomic elucidation of the function of such genes requires an understanding of the chemical ecology of the organism and, in particular, of the small molecules that act as selective agents either by promoting survival or causing selective mortality. In this overview, the significance of several groups of environmental response genes is examined in the context of chemical ecology. Cytochrome P-450 monooxygenases provide a case in point; these enzymes are involved in the biosynthesis of furanocoumarins (furocoumarins), toxic allelochemicals, in plants, as well as in their detoxification by lepidopterans. Biochemical innovations in insects and plants have historically been broadly defined in a coevolutionary context. Considerable insight can be gained by defining with greater precision components of those broad traits that contribute to diversification. Molecular approaches now allow chemical ecologists to characterize specifically those biochemical innovations postulated to lead to adaptation and diversification in plant/insect interactions.     

Chemical Ecology of Stingless Bees

Stingless bees (Hymenoptera, Apidae: Meliponini) represent a highly diverse group of social bees confined to the world’s tropics and subtropics. They show a striking diversity of structural and behavioral adaptations and are important pollinators of tropical plants. Despite their diversity and functional importance, their ecology, and especially chemical ecology, has received relatively little attention, particularly compared to their relative the honeybee, Apis mellifera. Here, I review various aspects of the chemical ecology of stingless bees, from communication over resource allocation to defense. I list examples in which functions of specific compounds (or compound groups) have been demonstrated by behavioral experiments, and show that many aspects (e.g., queen-worker interactions, host-parasite interactions, neuronal processing etc.) remain little studied. This review further reveals that the vast majority of studies on the chemical ecology of stingless bees have been conducted in the New World, whereas studies on Old World stingless bees are still comparatively rare. Given the diversity of species, behaviors and, apparently, chemical compounds used, I suggest that stingless bees provide an ideal subject for studying how functional context and the need for species specificity may interact to shape pheromone diversification in social insects.     

Heavy Metal Pollutants and Chemical Ecology: Exploring New Frontiers

Heavy metals are an important class of pollutants with both lethal and sublethal effects on organisms. The latter are receiving increased attention, as these may have harmful ecological outcomes. For example, recent explorations of heavy metals in freshwater habitats reveal that they can modify chemical communication between individuals, resulting in “info-disruption” that can impact ecological relationships within and between species. Info-disruption can affect animal behavior and social structure, which in turn can modify both intraspecies and interspecies interactions. In terrestrial habitats, info-disruption by metals is not well studied, but recent demonstrations of chemical signaling between plants via both roots and volatile organic molecules provide potential opportunities for info-disruption. Metals in terrestrial habitats also can form elemental plant defenses, in which they can defend a plant against natural enemies. For example, hyperaccumulation of metals by terrestrial plants has been shown to provide defensive benefits, although in almost all known cases the metals are not anthropogenic pollutants but are naturally present in soils inhabited by these plants. Info-disruption among microbes is another arena in which metal pollutants may have ecological effects, as recent discoveries regarding quorum sensing in bacteria provide an avenue for metals to affect interactions among bacteria or between bacteria and other organisms. Metal pollutants also may influence immune responses of organisms, and thus affect pathogen/host relationships. Immunomodulation (modification of immune system function) has been tied to some metal pollutants, although specific metals may boost or reduce immune system function depending on dose. Finally, the study of metal pollutants is complicated by their frequent occurrence as mixtures, either with other metals or with organic pollutants. Most studies of metal pollutants focus on single metals and therefore oversimplify complex field conditions. Study of pollutant impacts on chemical ecology also are difficult due to the necessity of studying effects at varying ecological scales: “dynamic scaling” of chemical ecology studies is rarely done completely. It is clear that much remains to be learned about how heavy metal pollution impacts organisms, and that exciting new research frontiers are available for experimental exploration.     

Effects of Arbuscular Mycorrhiza on Primary Metabolites in Phloem Exudates of Plantago major and Poa annua and on a Generalist Aphid

Arbuscular mycorrhiza (AM), i.e., the interaction of plants with arbuscular mycorrhizal fungi (AMF), often influences plant growth, physiology, and metabolism. Effects of AM on the metabolic composition of plant phloem sap may affect aphids. We investigated the impacts of AM on primary metabolites in phloem exudates of the plant species Plantago major and Poa annua and on the aphid Myzus persicae. Plants were grown without or with a generalist AMF species, leaf phloem exudates were collected, and primary metabolites were measured. Additionally, the performance of M. persicae on control and mycorrhizal plants of both species was assessed. While the plant species differed largely in the relative proportions of primary metabolites in their phloem exudates, metabolic effects of AM were less pronounced. Slightly higher proportions of sucrose and shifts in proportions of some amino acids in mycorrhizal plants indicated changes in phloem upload and resource allocation patterns within the plants. Aphids showed a higher performance on P. annua than on P. major. AM negatively affected the survival of aphids on P. major, whereas positive effects of AM were found on P. annua in a subsequent generation. Next to other factors, the metabolic composition of the phloem exudates may partly explain these findings.     

Does Aphid Infestation Interfere with Indirect Plant Defense against Lepidopteran Caterpillars in Wild Cabbage?

Attraction of parasitoids to plant volatiles induced by multiple herbivory depends on the specific combinations of attacking herbivore species, especially when their feeding modes activate different defense signalling pathways as has been reported for phloem feeding aphids and tissue feeding caterpillars. We studied the effects of pre-infestation with non-host aphids (Brevicoryne brassicae) for two different time periods on the ability of two parasitoid species to discriminate between volatiles emitted by plants infested by host caterpillars alone and those emitted by plants infested with host caterpillars plus aphids. Using plants originating from three chemically distinct wild cabbage (Brassica oleracea) populations, Diadegma semiclausum switched preference for dually infested plants to preference for plants infested with Plutella xylostella hosts alone when the duration of pre-aphid infestation doubled from 7 to 14 days. Microplitis mediator, a parasitoid of Mamestra brassicae caterpillars, preferred dually-infested plants irrespective of aphid-infestation duration. Separation of the volatile blends emitted by plants infested with hosts plus aphids or with hosts only was poor, based on multivariate statistics. However, emission rates of individual compounds were often reduced in plants infested with aphids plus hosts compared to those emitted by plants infested with hosts alone. This effect depended on host caterpillar species and plant population and was little affected by aphid infestation duration. Thus, the interactive effect of aphids and hosts on plant volatile production and parasitoid attraction can be dynamic and parasitoid specific. The characteristics of the multi-component volatile blends that determine parasitoid attraction are too complex to be deduced from simple correlative statistical analyses.     

Experience-Induced Habituation and Preference Towards Non-Host Plant Odors in Ovipositing Females of a Moth

In phytophagous insects, experience can increase positive responses towards non-host plant extracts or induce oviposition on non-host plants, but the underlying chemical and behavioral mechanisms are poorly understood. By using the diamondback moth, Plutella xylostella, its host plant Chinese cabbage, and a non-host plant Chrysanthemum morifolium, as a model system, we observed the experience-altered olfactory responses of ovipositing females towards volatiles of the non-host plant, volatiles of pure chemicals (p-cymene and α-terpinene) found in the non-host plant, and volatiles of host plants treated with these chemicals. We assessed the experience-altered oviposition preference towards host plants treated with p-cymene. Naive females showed aversion to the odors of the non-host plant, the pure chemicals, and the pure chemical-treated host plants. In contrast, experienced females either became attracted by these non-host odors or were no longer repelled by these odors. Similarly, naive females laid a significantly lower proportion of eggs on pure chemical-treated host plants than on untreated host plants, but experienced females laid a similar or higher proportion of eggs on pure chemical-treated host plants compared to untreated host plants. Chemical analysis indicated that application of the non-host pure chemicals on Chinese cabbage induced emissions of volatiles by this host plant. We conclude that induced preference for previously repellent compounds is a major mechanism that leads to behavioral changes of this moth towards non-host plants or their extracts.     

Pea Aphids, Acyrthosiphon Pisum, Suppress Induced Plant Volatiles in Broad Bean, Vicia Faba

Plants defend themselves against herbivory through several means, including the production of airborne volatile organic compounds (VOCs). These VOCs benefit plants by attracting natural enemies of their herbivores. The pea aphid, Acyrthosiphon pisum, is able to feed on its host plant, Vicia faba, without inducing detectable changes in plant VOC emission. Levels of VOCs emission are not significantly different between control plants and those fed upon by aphids for up to 5 days. Using a second herbivore, the beet armyworm caterpillar, Spodoptera exigua, we demonstrate that several expected caterpillar-induced VOCs are reduced when co-infested with pea aphids, thus demonstrating that pea aphids have the ability to inhibit the release of certain VOCs. This study shows, for the first time, that aphids not only avoid triggering plant volatile emission, but also can actively inhibit herbivore-induced volatiles.     

Variable diets and changing taste in plant-insect relationships

The host ranges of phytophagous insects are determined to a large degree by plant chemistry. Specialist insects are often closely associated with plants that produce characteristic chemicals, which may act as attractants or stimulants to aid in finding or recognizing a host. Generalist insects are generally believed to rely on the presence of repellents or deterrents to ensure avoidance of unsuitable plants. However, the chemistry of any plant can be highly variable, as a result of growth characteristics, genetic variation, or environmental factors. Such variable chemistry may provide windows of opportunity for nonadapted insects to utilize a plant or for a plant to become resistant to a normally adapted herbivore. Differences in insect responses to plant constituents may also result from genetic variation or environmental factors. In particular, dietary experience has been found to influence the ability of insects to taste plant chemicals that may serve as signals of suitability or unsuitability. Certain dietary constituents appear to suppress the development of taste sensitivity to deterrents in an insect, whereas the presence of specific stimulants in the diet may result in the development of dependence on these compounds. These findings further emphasize the fact that the dynamics of plant biochemistry along with plasticity in the sensory system of insects might be expected to play a major role in the evolution of new plant–insect relationships.     

Recent Progress Regarding the Molecular Aspects of Insect Gall Formation

Galls are characteristic plant structures formed by cell size enlargement and/or cell proliferation induced by parasitic or pathogenic organisms. Insects are a major inducer of galls, and insect galls can occur on plant leaves, stems, floral buds, flowers, fruits, or roots. Many of these exhibit unique shapes, providing shelter and nutrients to insects. To form unique gall structures, gall-inducing insects are believed to secrete certain effector molecules and hijack host developmental programs. However, the molecular mechanisms of insect gall induction and development remain largely unknown due to the difficulties associated with the study of non-model plants in the wild. Recent advances in next-generation sequencing have allowed us to determine the biological processes in non-model organisms, including gall-inducing insects and their host plants. In this review, we first summarize the adaptive significance of galls for insects and plants. Thereafter, we summarize recent progress regarding the molecular aspects of insect gall formation.     

Relative importance of semiochemicals from first and second trophic levels in host foraging behavior ofAphidius ervi

The responses of femaleAphidius ervi to odors from a host food plant (Vicia faba), host aphids (Acyrthosiphon pisum), nonhost aphids (Aphis fabae), and aphid-plant complexes were investigated in a specially designed wind tunnel and a Y-tube olfactometer. In single-target (no-choice) and two-target (dual-choice) experiments, plant volatiles played a crucial role in the host foraging behavior ofA. ervi. The odor from theA. pisum-plant complex elicited the strongest responses byA. ervi females, followed by the odor from plants previously damaged by the feeding ofA. pisum. There was a significantly weaker response to odor fromA. pisum in the absence of the plant and to undamaged plants. Similarly, mechanically damaged plants and plants infested with the nonhost aphidA. fabae did not elicit strong responses. A plant that had been damaged byA. pisum and subsequently washed with distilled water was as attractive as an unwashed, previously infested plant.Aphidius ervi probably overcomes the reliability-detectability problem by selectively responding to herbivore-induced, volatile, semiochemical cues emitted by the first trophic level and by distinguishing between the volatiles induced by host and nonhost aphids.     

Response of a Predatory ant to Volatiles Emitted by Aphid- and Caterpillar-Infested Cucumber and Potato Plants

In response to herbivory by insects, various plants produce volatiles that attract enemies of the herbivores. Although ants are important components of natural and agro-ecosystems, the importance of herbivore-induced plant volatiles (HIPVs) as cues for ants for finding food sources have received little attention. We investigated responses of the ant Formica pratensis to volatiles emitted by uninfested and insect-infested cucumber (Cucumis sativus) and potato (Solanum tuberosum) plants. Cucumber plants were infested by the phloem-feeding aphid Aphis gossypii, the leaf chewer Mamestra brassicae or simultaneously by both insects. Potato plants were infested by either Aphis gossypii, by the leaf chewer Chrysodeixis chalcites or both. In olfactometer experiments, ants preferred volatile blends emitted by cucumber plants infested with M. brassicae caterpillars alone or combined with A. gossypii to volatiles of undamaged plants or plants damaged by A. gossypii only. No preference was recorded in choice tests between volatiles released by aphid-infested plants over undamaged plants. Volatiles emitted by potato plants infested by either C. chalcites or A. gossypii were preferred by ants over volatiles released by undamaged plants. Ants did not discriminate between potato plants infested with aphids and caterpillars over plants infested with aphids only. Plant headspace composition showed qualitative and/or quantitative differences between herbivore treatments. Multivariate analysis revealed clear separation between uninfested and infested plants and among herbivore treatments. The importance of HIPVs in indirect plant defence by ants is discussed in the context of the ecology of ant-plant interactions and possible roles of ants in pest management.     

Molecular,Biochemical, and Organismal Analyses of Tomato Plants Simultaneously Attacked by Herbivores from Two Feeding Guilds

Previous work identified aphids and caterpillars as having distinct effects on plant responses to herbivory. We sought to decipher these interactions across different levels of biological organization, i.e., molecular, biochemical, and organismal, with tomato plants either damaged by one 3rd-instar beet armyworm caterpillar (Spodoptera exigua), damaged by 40 adult potato aphids (Macrosiphum euphorbiae), simultaneous damaged by both herbivores, or left undamaged (controls). After placing insects on plants, plants were transferred to a growth chamber for 5 d to induce a systemic response. Subsequently, individual leaflets from non-damaged parts of plants were excised and used for gene expression analysis (microarrays and quantitative real-time PCR), C/N analysis, total protein analysis, proteinase inhibitor (PI) analysis, and for performance assays. At the molecular level, caterpillars up-regulated 56 and down-regulated 29 genes systemically, while aphids up-regulated 93 and down-regulated 146 genes, compared to controls. Although aphids induced more genes than caterpillars, the magnitude of caterpillar-induced gene accumulation, particularly for those associated with plant defenses, was often greater. In dual-damaged plants, aphids suppressed 27% of the genes regulated by caterpillars, while caterpillars suppressed 66% of the genes regulated by aphids. At the biochemical level, caterpillars induced three-fold higher PI activity compared to controls, while aphids had no effects on PIs either alone or when paired with caterpillars. Aphid feeding alone reduced the foliar C/N ratio, but not when caterpillars also fed on the plants. Aphid and caterpillar feeding alone had no effect on the amount of protein in systemic leaves; however, both herbivores feeding on the plant reduced the amount of protein compared to aphid-damaged plants. At the organismal level, S. exigua neonate performance was negatively affected by prior caterpillar feeding, regardless of whether aphids were present or absent. This study highlights areas of concordance and disjunction between molecular, biochemical, and organismal measures of induced plant resistance when plants are attacked by multiple herbivores. In general, our data produced consistent results when considering each herbivore separately but not when considering them together.     

Chemotaxis of the Pinewood Nematode, <Emphasis Type="Italic">Bursaphelenchus xylophilus</Emphasis>, to Volatiles Associated with Host Pine, <Emphasis Type="Italic">Pinus massoniana</Emphasis>, and its Vector <Emphasis Type="Italic">Monochamus alternatus</Emphasis>

The pinewood nematode (PWN), Bursaphelenchus xylophilus, the most important invasive species in pine forests of Asia, is transported to new pine hosts by beetles of the genus Monochamus. Third-stage dispersal juveniles (J_III) aggregate in pupal chambers around the vector as it matures. We demonstrated that the ratio of three terpenes (α-pinene, β-pinene, and longifolene at 1:2.7:1.1) released by larval Monochamus alternatus strongly attract J_III, whereas the different ratio (1:0.1:0.01) of these three terpenes found in healthy xylem of Pinus massoniana attracts only the propagative stage (J_n) of the nematode. We suggest that the volatiles produced by the host plants could be the basis of a chemoecological relationship between plant parasitic nematodes and their vector insects. Capture of J_III with terpene-baited trap tubes deployed for 2 hr in the field was demonstrated. This technique may lead to the development of rapid sampling methodologies for use at either ports-of-entry or in the field.     

Diversity and Taxonomic Distribution of Endophytic Bacterial Community in the Rice Plant and Its Prospective

Endophytic bacterial communities are beneficial communities for host plants that exist inside the surfaces of plant tissues, and their application improves plant growth. They benefit directly from the host plant by enhancing the nutrient amount of the plant’s intake and influencing the phytohormones, which are responsible for growth promotion and stress. Endophytic bacteria play an important role in plant-growth promotion (PGP) by regulating the indirect mechanism targeting pest and pathogens through hydrolytic enzymes, antibiotics, biocontrol potential, and nutrient restriction for pathogens. To attain these benefits, firstly bacterial communities must be colonized by plant tissues. The nature of colonization can be achieved by using a set of traits, including attachment behavior and motility speed, degradation of plant polymers, and plant defense evasion. The diversity of bacterial endophytes colonization depends on various factors, such as plants’ relationship with environmental factors. Generally, each endophytic bacteria has a wide host range, and they are used as bio-inoculants in the form of synthetic applications for sustainable agriculture systems and to protect the environment from chemical hazards. This review discusses and explores the taxonomic distribution of endophytic bacteria associated with different genotypes of rice plants and their origin, movement, and mechanism of PGP. In addition, this review accentuates compressive meta data of endophytic bacteria communities associated with different genotypes of rice plants, retrieves their plant-growth-promoting properties and their antagonism against plant pathogens, and discusses the indication of endophytic bacterial flora in rice plant tissues using various methods. The future direction deepens the study of novel endophytic bacterial communities and their identification from rice plants through innovative techniques and their application for sustainable agriculture systems.     

Chemical Ecology Mediated by Fungal Endophytes in Grasses

Defensive mutualism is widely accepted as providing the best framework for understanding how seed-transmitted, alkaloid producing fungal endophytes of grasses are maintained in many host populations. Here, we first briefly review current knowledge of bioactive alkaloids produced by systemic grass-endophytes. New findings suggest that chemotypic diversity of the endophyte-grass symbiotum is far more complex, involving multifaceted signaling and chemical cross-talk between endophyte and host cells (e.g., reactive oxygen species and antioxidants) or between plants, herbivores, and their natural enemies (e.g., volatile organic compounds, and salicylic acid and jasmonic acid pathways). Accumulating evidence also suggests that the tight relationship between the systemic endophyte and the host grass can lead to the loss of grass traits when the lost functions, such as plant defense to herbivores, are compensated for by an interactive endophytic fungal partner. Furthermore, chemotypic diversity of a symbiotum appears to depend on the endophyte and the host plant life histories, as well as on fungal and plant genotypes, abiotic and biotic environmental conditions, and their interactions. Thus, joint approaches of (bio)chemists, molecular biologists, plant physiologists, evolutionary biologists, and ecologists are urgently needed to fully understand the endophyte-grass symbiosis, its coevolutionary history, and ecological importance. We propose that endophyte-grass symbiosis provides an excellent model to study microbially mediated multirophic interactions from molecular mechanisms to ecology.     

Experience Induces a Phytophagous Insect to Lay Eggs on a Nonhost Plant

Experience of nonhost plants by phytophagous insects may alter their foraging and oviposition responses to these plants. Using the diamondback moth (DBM) Plutella xylostella (L.), its host-plant Chinese cabbage, and a nonhost-plant Pisum sativum (pea) as a model system, we examined whether experience of the nonhost plant by adults can induce oviposition on the nonhost plant. Naive DBM females did not accept pea for oviposition in either no-choice or choice conditions, whereas females with prior experience of pea laid up to 20% of their eggs on this plant. Naive females reduced their oviposition, but experienced females did not refrain from laying eggs in a nonhost-plant environment. Such habituation to nonhost plants could lead to host range expansion in phytophagous insects and increase mortality of pest insects in diversified crop systems.     

Methyl Salicylate,a Soybean Aphid-Induced Plant Volatile Attractive to the Predator <Emphasis Type="Italic">Coccinella septempunctata</Emphasis>

Induced volatiles provide a signal to foraging predatory insects about the location of their prey. In Iowa, early in the growing season of soybean, Glycine max, many predacious seven-spotted lady beetles, Coccinella septempunctata, were observed on plants with heavy infestations of soybean aphid, Aphis glycines. We studied whether the attraction of this beetle is caused by the release of specific volatile compounds of soybean plants infested by aphids. Volatile compounds emitted by soybean plants infested by aphids were compared with those of undamaged, uninfested, and artificially damaged plants. Gas chromatography–mass spectrometry analyses revealed consistent differences in the profiles of volatile compounds between aphid-infested soybean plants and undamaged ones. Significantly more methyl salicylate was released from infested plants at both the V1 and V2 plant growth stages. However, release patterns of two other induced plant volatiles, (d)-limonene and (E,E)-α-farnesene, differed between the two plant growth stages. Gas chromatographic–electroantennographic detection of volatile extracts from infested soybean plants showed that methyl salicylate elicited significant electrophysiological responses in C. septempunctata. In field tests, traps baited with methyl salicylate were highly attractive to adult C. septempunctata, whereas 2-phenylethanol was most attractive to the lacewing Chrysoperla carnea and syrphid flies. Another common lady beetle, the multicolored Asian lady beetle, Harmonia axyridis, showed no preference for the compounds. These results indicate that C. septempunctata may use methyl salicylate as the olfactory cue for prey location. We also tested the attractiveness of some selected soybean volatiles to alate soybean aphids in the field, and results showed that traps baited with benzaldehyde caught significantly higher numbers of aphids.     

Host Plant Species Differentiation in a Polyphagous Moth: Olfaction is Enough

Polyphagous herbivorous insects need to discriminate suitable from unsuitable host plants in complex plant communities. While studies on the olfactory system of monophagous herbivores have revealed close adaptations to their host plant’s characteristic volatiles, such adaptive fine-tuning is not possible when a large diversity of plants is suitable. Instead, the available literature on polyphagous herbivore preferences suggests a higher level of plasticity, and a bias towards previously experienced plant species. It is therefore necessary to take into account the diversity of plant odors that polyphagous herbivores encounter in the wild in order to unravel the olfactory basis of their host plant choice behaviour. In this study we show that a polyphagous moth, Spodoptera littoralis, has the sensory ability to distinguish five host plant species using olfaction alone, this being a prerequisite to the ability to make a choice. We have used gas chromatography mass spectrometry (GC-MS) and gas chromatography electroantennographic detection (GC-EAD) in order to describe host plant odor profiles as perceived by S. littoralis. We find that each plant emits specific combinations and proportions of GC-EAD active volatiles, leading to statistically distinct profiles. In addition, at least four of these plants show GC-EAD active compound proportions that are conserved across individual plants, a characteristic that enables insects to act upon previous olfactory experiences during host plant choice. By identifying the volatiles involved in olfactory differentiation of alternative host plants by Spodoptera littoralis, we set the groundwork for deeper investigations of how olfactory perceptions translate into behaviour in polyphagous herbivores.