Molecular Rationale of Insect-Microbes Symbiosis—From Insect Behaviour to Mechanism

Insects nurture a panoply of microbial populations that are often obligatory and exist mutually with their hosts. Symbionts not only impact their host fitness but also shape the trajectory of their phenotype. This co-constructed niche successfully evolved long in the past to mark advanced ecological specialization. The resident microbes regulate insect nutrition by controlling their host plant specialization and immunity. It enhances the host fitness and performance by detoxifying toxins secreted by the predators and abstains them. The profound effect of a microbial population on insect physiology and behaviour is exploited to understand the host–microbial system in diverse taxa. Emergent research of insect-associated microbes has revealed their potential to modulate insect brain functions and, ultimately, control their behaviours, including social interactions. The revelation of the gut microbiota–brain axis has now unravelled insects as a cost-effective potential model to study neurodegenerative disorders and behavioural dysfunctions in humans. This article reviewed our knowledge about the insect–microbial system, an exquisite network of interactions operating between insects and microbes, its mechanistic insight that holds intricate multi-organismal systems in harmony, and its future perspectives. The demystification of molecular networks governing insect–microbial symbiosis will reveal the perplexing behaviours of insects that could be utilized in managing insect pests.

Lifelong exposure to artificial light at night impacts stridulation and locomotion activity patterns in the cricket Gryllus bimaculatus

Living organisms experience a worldwide continuous increase in artificial light at night (ALAN), negatively affecting their behaviour. The field cricket, an established model in physiology and behaviour, can provide insights into the effect of ALAN on insect behaviour. The stridulation and locomotion patterns of adult male crickets reared under different lifelong ALAN intensities were monitored simultaneously for five consecutive days in custom-made anechoic chambers. Daily activity periods and acrophases were compared between the experimental groups. Control crickets exhibited a robust rhythm, stridulating at night and demonstrating locomotor activity during the day. By contrast, ALAN affected both the relative level and timing of the crickets' nocturnal and diurnal activity. ALAN induced free-running patterns, manifested in significant changes in the median and variance of the activity periods, and even arrhythmic behaviour. The magnitude of disruption was light intensity dependent, revealing an increase in the difference between the activity periods calculated for stridulation and locomotion in the same individual. This finding may indicate the existence of two peripheral clocks. Our results demonstrate that ecologically relevant ALAN intensities affect crickets’ behavioural patterns, and may lead to decoupling of locomotion and stridulation behaviours at the individual level, and to loss of synchronization at the population level.

Electrical signalling on Bt and non-Bt cotton plants under stress by Aphis gossypii

Plants have developed various mechanisms to respond specifically to each biotrophic attack. It has been shown that the electrical signals emitted by plants are associated with herbivory stress responses and can lead to the activation of multiple defences. Bt cotton is a genetically modified pest-resistant plant that produces an insecticide from Bacillus thuringiensis (Bt) to control Lepidopteran species. Surprisingly, there is no study–yet, that characterizes the signalling mechanisms in transgenic cotton plants attacked by non-target insects, such as aphids. In this study, we characterized the production of electrical signals on Bt and non-Bt cotton plants infested with Aphis gossypii and, in addition, we characterized the dispersal behaviour of aphids to correlate this behaviour to plant signalling responses. Electrical signalling of the plants was recorded with an extracellular measurement technique. Impressively, our results showed that both Bt and non-Bt cotton varieties, when attacked by A. gossypii, emitted potential variation-type electrical signals and clearly showed the presence of distinct responses regarding their perception and the behaviour of aphids, with evidence of delay, in terms of signal amount, and almost twice the amount of Cry1F protein was observed on Bt cotton plants at the highest density of insects/plant. We present in our article some hypotheses that are based on plant physiology and insect behaviour to explain the responses found on Bt cotton plants under aphid stress.

Nocturnal city lighting elicits a macroscale response from an insect outbreak population

Anthropogenic environmental change affects organisms by exposing them to enhanced sensory stimuli that can elicit novel behavioural responses. A pervasive feature of the built environment is artificial nocturnal lighting, and brightly lit urban areas can influence organism abundance, distribution and community structure within proximate landscapes. In some cases, the attractive or disorienting effect of artificial light at night can draw animals into highly unfavourable habitats, acting as a macroscale attractive ecological sink. Despite their significance for animal ecology, identifying cases of these phenomena and determining their effective scales and the number of organisms impacted remains challenging. Using an integrated set of remote-sensing observations, we quantify the effect of a large-scale attractive sink on nocturnal flights of an outbreak insect population in Las Vegas, USA. At the peak of the outbreak, over 45 million grasshoppers took flight across the region, with the greatest numbers concentrating over high-intensity city lighting. Patterns of dusk ascent from vegetated habitat toward urban areas suggest a daily pull toward a time-varying nocturnal attractive sink. The strength of this attractor varies with grasshopper density. These observations provide the first macroscale characterization of the effects of nocturnal urban lighting on the behaviour of regional insect populations and demonstrate the link between insect perception of the built environment and resulting changes in spatial and movement ecology. As human-induced environmental change continues to affect insect populations, understanding the impacts of nocturnal light on insect behaviour and fitness will be vital to developing robust large-scale management and conservation strategies.

Crystal structure of Epiphyas postvittana pheromone binding protein 3

The insect olfactory system operates as a well-choreographed ensemble of molecules which functions to selectively translate volatile chemical messages present in the environment into neuronal impulses that guide insect behaviour. Of these molecules, binding proteins are believed to transport hydrophobic odorant molecules across the aqueous lymph present in antennal sensilla to receptors present in olfactory sensory neurons. Though the exact mechanism through which these proteins operate is still under investigation, these carriers clearly play a critical role in determining what an insect can smell. Binding proteins that transport important sex pheromones are colloquially named pheromone binding proteins (PBPs). Here, we have produced a functional recombinant PBP from the horticultural pest, Epiphyas postvittana (EposPBP3), and experimentally solved its apo-structure through X-ray crystallography to a resolution of 2.60 Å. Structural comparisons with related lepidopteran PBPs further allowed us to propose models for the binding of pheromone components to EposPBP3. The data presented here represent the first structure of an olfactory-related protein from the tortricid family of moths, whose members cause billions of dollars in losses to agricultural producers each year. Knowledge of the structure of these important proteins will allow for subsequent studies in which novel, olfactory molecule-specific insecticides can be developed.

Vector manipulation by a semi-persistent plant virus through disease symptom expression

The greenhouse whitefly (GWF), Trialeurodes vaporariorum (Westwood) (Hemiptera: Aleyrodidae) is rarely associated with potato plants yet is the only known vector of the Potato yellow vein virus (PYVV). A host shift related with vector’s cognition often requires neural alterations by the virus. However, PYVV, being semi-persistent, is not supposed to directly affect vector physiology. As such, we propose that changes in potato plants caused by PYVV infection should manipulate insect behaviour to increase transmission. Here, we studied the effect of PYVV infection and symptom expression on GWF biological parameters, and attraction towards infected and uninfected potato plants. We compared survival and development rates of GWF nymphs fed with PYVV-infected plants (symptomatic and asymptomatic) and healthy plants under controlled conditions. We also carried out free-choice tests to determine host preference of GWF adults as a function of PYVV infection and disease symptom expression. We found that PYVV infection (both symptomatic and asymptomatic) reduce GWF survival while increasing development time (in symptomatic plants). Combined, a prolonged development time and reduced survival should favour viral uptake and trigger migration of vectors from symptomatic plants short after acquiring the virus. We also found that symptom expression (yellowing) causes significantly greater GWF attraction and establishment compared to healthy or asymptomatic plants. Interestingly, we found that GWF adults that have previously fed on infected plants switch their host preference choosing and establishing on healthy potato plants, which clearly increases horizontal transmission rates. The mechanism through which this behavioural manipulation takes place is not yet well understood. Our results show that symptoms associated with PYVV infection may account for a set of behavioural modifications that make an improbable vector, such as the GWF, into an efficient agent that increases horizontal transmission rates of PYVV.HighlightsPYVD reduces the survival of GWF and increases development time when symptoms occurPYVD symptom makes potato, a non-host plant, attractive to GWFAfter feeding on infected plants, GWF preference changes to prefer uninfected plantsPYVV modulates GWF behaviour to enhance horizontal transmission between plants

Floral vibrations by buzz-pollinating bees achieve higher frequency, velocity and acceleration than flight and defence vibrations

Vibrations play an important role in insect behaviour. In bees, vibrations are used in a variety of contexts including communication, as a warning signal to deter predators and during pollen foraging. However, little is known about how the biomechanical properties of bee vibrations vary across multiple behaviours within a species. In this study, we compared the properties of vibrations produced by Bombus terrestris audax (Hymenoptera: Apidae) workers in three contexts: during flight, during defensive buzzing, and in floral vibrations produced during pollen foraging on two buzz-pollinated plants (Solanum, Solanaceae). Using laser vibrometry, we were able to obtain contactless measures of both the frequency and amplitude of the thoracic vibrations of bees across the three behaviours. Despite all three types of vibrations being produced by the same power flight muscles, we found clear differences in the mechanical properties of the vibrations produced in different contexts. Both floral and defensive buzzes had higher frequency and amplitude velocity, acceleration, and displacement than the vibrations produced during flight. Floral vibrations had the highest frequency, amplitude velocity and acceleration of all the behaviours studied. Vibration amplitude, and in particular acceleration, of floral vibrations has been suggested as the key property for removing pollen from buzz-pollinated anthers. By increasing frequency and amplitude velocity and acceleration of their vibrations during vibratory pollen collection, foraging bees may be able to maximise pollen removal from flowers, although their foraging decisions are likely to be influenced by the presumably high cost of producing floral vibrations.