Search

Significance India is the world’s largest fruit producer and second most populous country. Pollinators are therefore important for India’s food security. India also contains 9 of the world’s 10 most polluted cities, but the impact of air pollution on plant and animal systems is largely unknown. We performed a multiyear study in the megacity of Bangalore to correlate the mechanistic effects of air pollution on a major Indian pollinator, the Giant Asian honey bee, Apis dorsata. Wild honey bees and lab-reared Drosophila exposed to air pollution exhibited differences in survival, behavior, heart rate, blood cell count, and/or the expression of genes related to stress, immunity, and metabolism. Our study indicates the urgency for more studies on wild systems to better inform international air quality guidelines., While the impact of air pollution on human health is well studied, mechanistic impacts of air pollution on wild systems, including those providing essential ecosystem services, are largely unknown, but directly impact our health and well-being. India is the world’s largest fruit producer, second most populous country, and contains 9 of the world’s 10 most polluted cities. Here, we sampled Giant Asian honey bees, Apis dorsata, at locations with varying air pollution levels in Bangalore, India. We observed significant correlations between increased respirable suspended particulate matter (RSPM) deposition and changes in bee survival, flower visitation, heart rate, hemocyte levels, and expression of genes related to lipid metabolism, stress, and immunity. Lab-reared Drosophila melanogaster exposed to these same sites also exhibited similar molecular and physiological differences. Our study offers a quantitative analysis on the current impacts of air pollution on insects, and indicates the urgency for more nonhuman studies to accurately assess the effects of pollution on our natural world.

Significance Flying insects are Earth’s most diverse taxonomic class. They exhibit remarkable abilities to locate resources while flying through complex 3D environments. However, we still have not deciphered how flying insects integrate multiple stimuli and extract depth to locate distant targets. Here, we assessed long-range search behavior in tethered flies using virtual reality. We first show that insects of multiple species can navigate to virtual 3D objects. We then show flies can employ perspective and motion parallax to distinguish size and distance amidst a complex background, and can incorporate directional airflow and odor to navigate toward distant targets. These results provide the foundation to elucidate search processes for pest management, pollination, and dispersal, and apply them to robotics and search algorithms., The exemplary search capabilities of flying insects have established them as one of the most diverse taxa on Earth. However, we still lack the fundamental ability to quantify, represent, and predict trajectories under natural contexts to understand search and its applications. For example, flying insects have evolved in complex multimodal three-dimensional (3D) environments, but we do not yet understand which features of the natural world are used to locate distant objects. Here, we independently and dynamically manipulate 3D objects, airflow fields, and odor plumes in virtual reality over large spatial and temporal scales. We demonstrate that flies make use of features such as foreground segmentation, perspective, motion parallax, and integration of multiple modalities to navigate to objects in a complex 3D landscape while in flight. We first show that tethered flying insects of multiple species navigate to virtual 3D objects. Using the apple fly Rhagoletis pomonella, we then measure their reactive distance to objects and show that these flies use perspective and local parallax cues to distinguish and navigate to virtual objects of different sizes and distances. We also show that apple flies can orient in the absence of optic flow by using only directional airflow cues, and require simultaneous odor and directional airflow input for plume following to a host volatile blend. The elucidation of these features unlocks the opportunity to quantify parameters underlying insect behavior such as reactive space, optimal foraging, and dispersal, as well as develop strategies for pest management, pollination, robotics, and search algorithms.

Changes in behaviour often drive rapid adaptive evolution and speciation. However, the mechanistic basis for behavioural shifts is largely unknown. The tephritid fruit fly Rhagoletis pomonella is an example of ecological specialization and speciation in action via a recent host plant shift from hawthorn to apple. These flies primarily use specific odours to locate fruit, and because they mate only on or near host fruit, changes in odour preference for apples versus hawthorns translate directly to prezygotic reproductive isolation, initiating speciation. Using a variety of techniques, we found a reversal between apple and hawthorn flies in the sensory processing of key odours associated with host fruit preference at the first olfactory synapse, linking changes in the antennal lobe of the brain with ongoing ecological divergence. Indeed, changes to specific neural pathways of any sensory modality may be a broad mechanism for changes in animal behaviour, catalysing the genesis of new biodiversity.

Significance The coeveolution of flowers and pollinators is well known, but how generalist pollinators identify suitable flowers across environments and flower species is not well understood. Hoverflies, which are found across the globe, are one of the most important alternative pollinators after bees and bumblebees. Here we measured, predicted, and finally recreated multimodal cues from individual flowers visited by hoverflies in three different environments (hemiboreal, alpine, and tropical). We found that although “flower signatures” were unique for each environment, some cues were ubiquitously attractive, despite not resembling cue combinations from real flowers. Our results provide unique insights into how a cosmopolitan pollinator identifies flower objects across environments, which has important implications for our understanding of pollination as a global ecological service., With more than 80% of flowering plant species specialized for animal pollination, understanding how wild pollinators utilize resources across environments can encourage efficient planting and maintenance strategies to maximize pollination and establish resilience in the face of environmental change. A fundamental question is how generalist pollinators recognize “flower objects” in vastly different ecologies and environments. On one hand, pollinators could employ a specific set of floral cues regardless of environment. Alternatively, wild pollinators could recognize an exclusive signature of cues unique to each environment or flower species. Hoverflies, which are found across the globe, are one of the most ecologically important alternative pollinators after bees and bumblebees. Here, we have exploited their cosmopolitan status to understand how wild pollinator preferences change across different continents. Without employing any a priori assumptions concerning the floral cues, we measured, predicted, and finally artificially recreated multimodal cues from individual flowers visited by hoverflies in three different environments (hemiboreal, alpine, and tropical) using a field-based methodology. We found that although “flower signatures” were unique for each environment, some multimodal lures were ubiquitously attractive, despite not carrying any reward, or resembling real flowers. While it was unexpected that cue combinations found in real flowers were not necessary, the robustness of our lures across insect species and ecologies could reflect a general strategy of resource identification for generalist pollinators. Our results provide insights into how cosmopolitan pollinators such as hoverflies identify flowers and offer specific ecologically based cues and strategies for attracting pollinators across diverse environments.

Recent studies have shown that flies from sympatric populations of Rhagoletis pomonella infesting hawthorn, apple, and flowering dogwood fruit can distinguish among unique volatile blends identified from each host. Analysis of peripheral chemoreception in Rhagoletis flies suggests that changes in receptor specificity and/or receptor neuron sensitivity could impact olfactory preference among the host populations and their hybrids. In an attempt to validate these claims, we have combined flight tunnel analyses and single sensillum electrophysiology in F(2) and backcross hybrids displaying a variety of behavioral phenotypes. Results show that differences in peripheral chemoreception among second-generation adults do not provide a direct correlation between peripheral coding and olfactory behavior. We conclude that either the plasticity of the central nervous system in Rhagoletis can compensate for significant alterations in peripheral coding or that peripheral changes present subtle effects on behavior not easily detectable with current techniques. The results of this study imply that the basis for olfactory behavior in Rhagoletis has a complicated genetic and neuronal basis, even for populations with a recent divergence in preference.

In this issue of Chemical Senses, Baker et al. propose a provocative and intriguing explanation for a commonly observed phenomenon in moth chemocommunication. Sex pheromones in moths typically consist of mixtures of long-chain unsaturated compounds in specific ratios. These ratios are correspondingly detected by male moths using separate olfactory sensory neurons for each pheromone component housed singly or multiply in long trichoid sensilla on the antennal surface. These neurons are often present in different proportions, typically with the neuron responding to the highest ratio component present in greatest abundance or with the largest dendritic diameter. In their article, Baker et al. postulate that these physical differences in neuron magnitudes arise to compensate for the higher molecular flux present with the most abundant pheromone components. Such a suggestion raises several questions concerning the physiological and behavioral nature of pheromone communication. Specifically, is the flux in a natural pheromone plume high enough to warrant increased flux detection for the most abundant components? Second, how can changes in neuronal number or size lead to increased flux detection? And finally, how would this increased flux detection be accomplished at molecular, cellular, and ultimately network scales? We address each of these questions and propose future experiments that could offer insight into the stimulating proposition raised by Baker et al.

The reproductive success of herbivorous insects largely depends on the mother’s oviposition preference. In nocturnal insects, olfaction is arguably the most important sensory modality mediating mate finding, foraging, and host location. In most habitats, gravid females select among a number of plants of varying suitability, yet assessment of the neuroethological mechanisms underlying odor-guided choice between host plants is rare. Using a series of behavioral, electrophysiological, and chromatographic analyses in the Hawk moth, Manduca sexta, we show that gravid females perform a hierarchical choice among host plants of different species and qualities using olfactory cues. Both relevant plant species and qualities can be distinguished by volatile profiles collected from the headspace of these plants, and olfactory sensilla on female antennae detect more than half of the about 120 analytically detected volatiles in host plant headspace samples. Although olfactory sensory neurons present in antennal sensilla are mainly broadly tuned to multiple host compounds, some sensilla exhibit species and condition-specific responses. In fact, species and quality can be distinguished by the physiologically active components alone. Our findings thus suggest that distinguishing characteristics of both host species and quality are already represented at the sensory periphery.

Behavioural changes in habitat or mate choice can trigger population divergence, leading to speciation. However, little is known about the neurological bases for such changes. Rhagoletis pomonella (Diptera: Tephritidae) is a model for ecological speciation via host plant shifts. Within the past 180 years, Rhagoletis flies infesting hawthorn ( Crataegus spp.) shifted to attack domesticated apple ( Malus pumila ). The two populations differ in their olfactory preferences for apple versus hawthorn fruit. Here, we looked for patterns of sensory organization that may have contributed to this shift by characterizing the morphology, specificity and distribution of olfactory sensory neurons (OSNs) on the antennae of Rhagoletis responding to host fruit and non-host volatiles. Of 28 OSN classes identified, two colocalized OSN pairs were found that specifically responded to the major behavioural attractant and antagonist volatiles for each fly population. A reversal in the response of these OSNs to fruit volatiles, either through a switch in receptor expression between these paired neurons or changes in neuronal projections in the brain, could therefore account for the behavioural difference between apple and hawthorn flies. The finding supports the hypothesis that relatively minor changes in olfactory sensory pathways may contribute to rapid host shifting and divergence in Rhagoletis .

The Rhagoletis species complex has been a key player in the sympatric speciation debate for much of the last 50 years. Studies indicate that differences in olfactory preference for host fruit volatiles could be important in reproductively isolating flies infesting each type of fruit via premating barriers to gene flow. Single sensillum electrophysiology was used to compare the response characteristics of olfactory receptor neurons from apple, hawthorn, and flowering dogwood-origin populations of R. pomonella, as well as from the blueberry maggot, R. mendax (an outgroup). Eleven volatiles were selected as stimuli from behavioral/electroantennographic studies of the three R. pomonella host populations. Previously, we reported that differences in preference for host fruit volatile blends are not a function of alterations in the general class of receptor neurons tuned to key host volatiles. In the present study, population comparisons involving dose–response trials with the key volatiles revealed significant variability in olfactory receptor neuron sensitivity and temporal firing pattern both within and among Rhagoletis populations. It is concluded that such variability in peripheral sensitivity and temporal firing pattern could influence host preference and contribute to host fidelity and sympatric host shifts in the Rhagoletis complex.