Social bees are important insect pollinators of wildflowers and agricultural crops, making their reported declines a global concern. A major factor implicated in these declines is the widespread use ...of neonicotinoid pesticides. Indeed, recent research has demonstrated that exposure to low doses of these neurotoxic pesticides impairs bee behaviours important for colony function and survival. However, our understanding of the molecular‐genetic pathways that lead to such effects is limited, as is our knowledge of how effects may differ between colony members. To understand what genes and pathways are affected by exposure of bumblebee workers and queens to neonicotinoid pesticides, we implemented a transcriptome‐wide gene expression study. We chronically exposed Bombus terrestriscolonies to either clothianidin or imidacloprid at field‐realistic concentrations while controlling for factors including colony social environment and worker age. We reveal that genes involved in important biological processes including mitochondrial function are differentially expressed in response to neonicotinoid exposure. Additionally, clothianidin exposure had stronger effects on gene expression amplitude and alternative splicing than imidacloprid. Finally, exposure affected workers more strongly than queens. Our work demonstrates how RNA‐Seq transcriptome profiling can provide detailed novel insight on the mechanisms mediating pesticide toxicity to a key insect pollinator.
Annual social insects are an integral functional group of organisms, particularly in temperate environments. An emblematic part of their annual cycle is the social phase, during which the ...colony-founding queen rears workers that later assist her in rearing sexual progeny (gynes and drones). In many annual social insects, such as species of bees, wasps, and other groups, developing larvae are provisioned gradually as they develop (progressive provisioning) leading to multiple larval generations being reared simultaneously. We present a model for how the queen in such cases should optimize her egg-laying rate throughout the social phase depending on number-size trade-offs, colony age-structure, and energy balance. Complementing previous theory on optimal allocation between workers vs. sexuals in annual social insects and on temporal egg-laying patterns in solitary insects, we elucidate how resource competition among overlapping larval generations can influence optimal egg-laying strategies. With model parameters informed by knowledge of a common bumblebee species, the optimal egg-laying schedule consists of two temporally separated early broods followed by a more continuous rearing phase, matching empirical observations. However, eggs should initially be laid continuously at a gradually increasing rate when resources are scarce or mortality risks high and in cases where larvae are fully supplied with resources at the egg-laying stage (mass-provisioning). These factors, alongside sexual:worker body size ratios, further determine the overall trend in egg-laying rates over the colony cycle. Our analysis provides an inroad to study and mechanistically understand variation in colony development strategies within and across species of annual social insects.
Social bees represent an important group of pollinating insects that can be exposed to potentially harmful pesticides when foraging on treated or contaminated flowering plants. To investigate if such ...exposure is detrimental to bees, many studies have exclusively fed individuals with pesticide-spiked food, informing us about the hazard but not necessarily the risk of exposure. While such studies are important to establish the physiological and behavioural effects on individuals, they do not consider the possibility that the risk of exposure may change over time. For example, many pesticide assays exclude potential behavioural adaptations to novel toxins, such as rejection of harmful compounds by choosing to feed on an uncontaminated food source, thus behaviourally lowering the risk of exposure. In this paper, we conducted an experiment over 10 days in which bumblebees could forage on an array of sucrose feeders containing 0, 2 and 11 parts per billion of the neonicotinoid pesticide thiamethoxam. This more closely mimics pesticide exposure in the wild by allowing foraging bees to (i) experience a field realistic range of pesticide concentrations across a chronic exposure period, (ii) have repeated interactions with the pesticide in their environment, and (iii) retain the social cues associated with foraging by using whole colonies. We found that the proportion of visits to pesticide-laced feeders increased over time, resulting in greater consumption of pesticide-laced sucrose relative to untreated sucrose. After changing the spatial position of each feeder, foragers continued to preferentially visit the pesticide-laced feeders which indicates that workers can detect thiamethoxam and alter their behaviour to continue feeding on it. The increasing preference for consuming the neonicotinoid-treated food therefore increases the risk of exposure for the colony during prolonged pesticide exposure. Our results highlight the need to incorporate attractiveness of pesticides to foraging bees (and potentially other insect pollinators) in addition to simply considering the proportion of pesticide-contaminated floral resources within the foraging landscape.
For social bees, an understudied step in evaluating pesticide risk is how contaminated food entering colonies affects residing offspring development and maturation. For instance, neurotoxic ...insecticide compounds in food could affect central nervous system development predisposing individuals to become poorer task performers later-in-life. Studying bumblebee colonies provisioned with neonicotinoid spiked nectar substitute, we measured brain volume and learning behaviour of 3 or 12-day old adults that had experienced in-hive exposure during brood and/or early-stage adult development. Micro-computed tomography scanning and segmentation of multiple brain neuropils showed exposure during either of the developmental stages caused reduced mushroom body calycal growth relative to unexposed workers. Associated with this was a lower probability of responding to a sucrose reward and lower learning performance in an olfactory conditioning test. While calycal volume of control workers positively correlated with learning score, this relationship was absent for exposed workers indicating neuropil functional impairment. Comparison of 3- and 12-day adults exposed during brood development showed a similar degree of reduced calycal volume and impaired behaviour highlighting lasting and irrecoverable effects from exposure despite no adult exposure. Our findings help explain how the onset of pesticide exposure to whole colonies can lead to lag-effects on growth and resultant dysfunction.
1. Pesticide exposure has been implicated as a contributor to insect pollinator declines. In social bees, which are crucial pollination service providers, the effect of low-level chronic exposure is ...typically non-lethal leading researchers to consider whether exposure induces sublethal effects on behaviour and whether such impairment can affect colony development. 2. Studies under laboratory conditions can control levels of pesticide exposure and elucidate causative effects, but are often criticized for being unrealistic. In contrast, field studies can monitor bee responses under a more realistic pesticide exposure landscape; yet typically such findings are limited to correlative results and can lack true controls or sufficient replication. We attempt to bridge this gap by exposing bumblebees to known amounts of pesticides when colonies are placed in the field. 3. Using 20 bumblebee colonies, we assess the consequences of exposure to the neonicotinoid clothianidin, provided in sucrose at a concentration of five parts per billion, over 5 weeks. We monitored foraging patterns and pollen collecting performance from 3282 bouts using either a non-invasive photographic assessment, or by extracting the pollen from returning foragers. We also conducted a full colony census at the beginning and end of the experiment. 4. In contrast to studies on other neonicotinoids, showing clear impairment to foraging behaviours, we detected only subtle changes to patterns of foraging activity and pollen foraging during the course of the experiment. However, our colony census measures showed a more pronounced effect of exposure, with fewer adult workers and sexuals in treated colonies after 5 weeks. 5. Synthesis and applications. Pesticide-induced impairments on colony development and foraging could impact on the pollination service that bees provide. Therefore, our findings, that bees show subtle changes in foraging behaviour and reductions in colony size after exposure to a common pesticide, have important implications and help to inform the debate over whether the benefits of systemic pesticide application to flowering crops outweigh the costs. We propose that our methodology is an important advance to previous semi-field methods and should be considered when considering improvements to current ecotoxicological guidelines for pesticide risk assessment.
Abstract
Environmental changes threaten insect pollinators, creating risks for agriculture and ecosystem stability. Despite their importance, we know little about how wild insects respond to ...environmental pressures. To understand the genomic bases of adaptation in an ecologically important pollinator, we analyzed genomes of Bombus terrestris bumblebees collected across Great Britain. We reveal extensive genetic diversity within this population, and strong signatures of recent adaptation throughout the genome affecting key processes including neurobiology and wing development. We also discover unusual features of the genome, including a region containing 53 genes that lacks genetic diversity in many bee species, and a horizontal gene transfer from a Wolbachia bacteria. Overall, the genetic diversity we observe and how it is distributed throughout the genome and the population should support the resilience of this important pollinator species to ongoing and future selective pressures. Applying our approach to more species should help understand how they can differ in their adaptive potential, and to develop conservation strategies for those most at risk.
Insect declines are a global issue with significant ecological and economic ramifications. Yet, we have a poor understanding of the genomic impact these losses can have. Genome‐wide data from ...historical specimens have the potential to provide baselines of population genetic measures to study population change, with natural history collections representing large repositories of such specimens. However, an initial challenge in conducting historical DNA data analyses is to understand how molecular preservation varies between specimens.
Here, we highlight how Next‐Generation Sequencing methods developed for studying archaeological samples can be applied to determine DNA preservation from only a single leg taken from entomological museum specimens, some of which are more than a century old. An analysis of genome‐wide data from a set of 113 red‐tailed bumblebee Bombus lapidarius specimens, from five British museum collections, was used to quantify DNA preservation over time. Additionally, to improve our analysis and further enable future research, we generated a novel assembly of the red‐tailed bumblebee genome.
Our approach shows that museum entomological specimens are comprised of short DNA fragments with mean lengths below 100 base pairs (BP), suggesting a rapid and large‐scale post‐mortem reduction in DNA fragment size. After this initial decline, however, we find a relatively consistent rate of DNA decay in our dataset, and estimate a mean reduction in fragment length of 1.9 bp per decade. The proportion of quality filtered reads mapping to our assembled reference genome was around 50%, and decreased by 1.1% per decade.
We demonstrate that historical insects have significant potential to act as sources of DNA to create valuable genetic baselines. The relatively consistent rate of DNA degradation, both across collections and through time, mean that population‐level analyses—for example for conservation or evolutionary studies—are entirely feasible, as long as the degraded nature of DNA is accounted for.
Offspring of many animals develop in environments in which they are exposed to high densities of potentially harmful bacteria. For example, larvae of the carrion beetle Nicrophorus vespilloides face ...significant challenges from the bacteria they encounter during their development on decomposing vertebrate carcasses. We tested the idea that larvae secrete antimicrobial compounds during development to defend themselves against microbial exposure. We first showed that larval secretion of active antimicrobials peaked during the early stages of development. As has been found previously for parental secretions, larval secretions were active against Gram-positive but not Gram-negative bacteria, indicating that they might be based on lysozyme-like compounds. Finally, consistent with this antibacterial activity, we showed that larval survival declined significantly when challenged with lysozyme-resistant Staphylococcus aureus but not when challenged with a lysozyme-susceptible strain of the same species. These results demonstrate that Nicrophorus larvae are not simply passive recipients of social immunity derived from their parents, but that they are active participants in its production.
•Nicrophorus vespilloides larvae secrete lytic compounds early in development.•Larval secretions are similar in function to those secreted by adults during breeding.•Variation in lytic activity creates potential conflicts over secretion production.•By producing secretions larvae contribute to resource defence and social immunity.
Determining when animal populations have experienced stress in the past is fundamental to understanding how risk factors drive contemporary and future species' responses to environmental change. For ...insects, quantifying stress and associating it with environmental factors has been challenging due to a paucity of time‐series data and because detectable population‐level responses can show varying lag effects. One solution is to leverage historic entomological specimens to detect morphological proxies of stress experienced at the time stressors emerged, allowing us to more accurately determine population responses.
Here we studied specimens of four bumblebee species, an invaluable group of insect pollinators, from five museums collected across Britain over the 20th century. We calculated the degree of fluctuating asymmetry (FA; random deviations from bilateral symmetry) between the right and left forewings as a potential proxy of developmental stress.
We: (a) investigated whether baseline FA levels vary between species, and how this compares between the first and second half of the century; (b) determined the extent of FA change over the century in the four bumblebee species, and whether this followed a linear or nonlinear trend; (c) tested which annual climatic conditions correlated with increased FA in bumblebees.
Species differed in their baseline FA, with FA being higher in the two species that have recently expanded their ranges in Britain. Overall, FA significantly increased over the century but followed a nonlinear trend, with the increase starting c. 1925. We found relatively warm and wet years were associated with higher FA.
Collectively our findings show that FA in bumblebees increased over the 20th century and under weather conditions that will likely increase in frequency with climate change. By plotting FA trends and quantifying the contribution of annual climate conditions on past populations, we provide an important step towards improving our understanding of how environmental factors could impact future populations of wild beneficial insects.
Determining stress events improves our understanding of the drivers of population declines, but a lack of baseline data makes this challenging. Leveraging museum specimens, the authors measured the change in bumblebee wing‐shape fluctuating asymmetry (FA; proxy of stress) between 1900 and 2000. FA increased over the century, with warmer, wetter conditions predicting higher FA.
Agricultural intensification has drastically altered foraging landscapes for bees, with large-scale crop monocultures associated with floral diversity loss. Research on bumblebees and honeybees has ...shown individuals feeding on pollen from a low richness of floral sources can experience negative impacts on health and longevity relative to higher pollen source richness of similar protein concentrations. Florally rich landscapes are thus generally assumed to better support social bees. Yet, little is known about whether the effects of reduced pollen source richness can be mitigated by feeding on pollen with higher crude protein concentration, and importantly how variation in diet affects whole colony growth, rearing decisions and sexual production. Studying queen-right bumblebee (
) colonies, we monitored colony development under a polyfloral pollen diet or a monofloral pollen diet with 1.5-1.8 times higher crude protein concentration. Over 6 weeks, we found monofloral colonies performed better for all measures, with no apparent long-term effects on colony mass or worker production, and a higher number of pupae in monofloral colonies at the end of the experiment. Unexpectedly, polyfloral colonies showed higher mortality, and little evidence of any strategy to counteract the effects of reduced protein; with fewer and lower mass workers being reared, and males showing a similar trend. Our findings (i) provide well-needed daily growth dynamics of queenright colonies under varied diets, and (ii) support the view that pollen protein content in the foraging landscape rather than floral species richness
is likely a key driver of colony health and success.
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