Annual Review of Entomology

Biological Control of Aphids in China: Successes and Prospects
Liu TX and Chen XX
Aphids are small, soft-bodied insects, and many are notorious pests of field crops, vegetables, fruit trees, ornamental plants, and trees. In China, there is an increasing emphasis on utilizing biological control agents, including aphidopathogenics, and selective pesticides for the management of aphids. In particular, preventive integrated pest management strategies with early interventions reduce the financial and environmental costs associated with treatments of outbreaks. Decades of progress have proved that biological control is a cost-effective and environmentally safe control option. Here, we review the history and progress of aphid control, with an emphasis on major natural enemies, mass-rearing, and conservation, and provide two successful cases, constraints, and future perspectives on aphid biological control in China.
The East Asian Insect Flyway: Geographical and Climatic Factors Driving Migration Among Diverse Crop Pests
Hu G, Feng H, Otuka A, Reynolds DR, Drake VA and Chapman JW
The East Asian Insect Flyway is a globally important migration route stretching from the Indochina Peninsula and the Philippines through East China to Northeast China and northern Japan, although most migrants utilize only part of the flyway. In this review, we focus on long-range windborne migrations of lepidopteran and planthopper pests. We outline the environment in which migrations occur, with emphasis on the seasonal atmospheric circulations that influence the transporting wind systems. Northward movement in spring is facilitated by favorable prevailing winds, allowing migrants to colonize vast areas of East Asia. Migrants may be subject to contemporary natural selection for long flights as succeeding generations progressively advance northward. Overshooting into far northern areas from which there is little chance of return seems common in planthoppers. Moths are less profligate and have evolved complex flight behaviors that can facilitate southward transport in autumn, although timely spells of favorable winds may not occur in some years.
Effects of Elevated CO and O on Aboveground Brassicaceous Plant-Insect Interactions
Bede JC and Blande JD
Atmospheric gases, such as carbon dioxide (CO) and ozone (O), influence plant-insect interactions, with variable effects. The few studies that have investigated the direct effects of elevated CO (eCO; 750-900 ppm) or elevated O (eO; 60-200 ppb) on insects have shown mixed results. Instead, most research has focused on the indirect effects through changes in the host plant. In general, the lower nitrogen levels in C3 brassicaceous plants grown at eCO negatively affect insects and may result in compensatory feeding. Phytohormones involved in plant resistance may be altered by eCO or eO. For example, stress-related jasmonate levels, which lead to induced resistance against chewing herbivores, are weakened at eCO. In general, eCO does not affect herbivore-induced plant volatiles, which remain attractive to natural enemies. However, floral volatiles and herbivore-induced plant volatiles may be degraded by O, affecting pollination and foraging natural enemy behavior. Thus, eCO and eO alter plant-insect interactions; however, many aspects remain poorly understood.
Gene Drive and Symbiont Technologies for Control of Mosquito-Borne Diseases
Wang GH, Hoffmann A and Champer J
Mosquito-borne diseases, such as dengue and malaria, pose a significant burden to global health. Current control strategies with insecticides are only moderately effective. Scalable solutions are needed to reduce the transmission risk of these diseases. Symbionts and genome engineering-based mosquito control strategies have been proposed to address these problems. Bacterial, fungal, and viral symbionts affect mosquito reproduction, reduce mosquito lifespan, and block pathogen transmission. Field tests of endosymbiont -based methods have yielded promising results, but there are hurdles to overcome due to the large-scale rearing and accurate sex sorting required for -based suppression approaches and the ecological impediments to invasion in replacement approaches. Genome engineering-based methods, in which mosquitoes are genetically altered for the modification or suppression of wild populations, offer an additional approach for control of mosquito-borne diseases. In particular, the use of gene drive alleles that bias inheritance in their favor is a potentially powerful approach. Several drives are frequency dependent, potentially giving them broadly similar population dynamics to . However, public acceptance and the behavior of released drives in natural mosquito populations remain challenges. We summarize the latest developments and discuss the knowledge gaps in both symbiont- and gene drive-based methods.
Illuminating Entomological Dark Matter with DNA Barcodes in an Era of Insect Decline, Deep Learning, and Genomics
Meier R, Lawniczak MKN and Srivathsan A
Most insects encountered in the field are initially entomological dark matter in that they cannot be identified to species while alive. This explains the enduring quest for efficient ways to identify collected specimens. Morphological tools came first but are now routinely replaced or complemented with DNA barcodes. Initially too expensive for widespread use, these barcodes have since evolved into powerful tools for specimen identification and sorting, given that the evolution of sequencing approaches has dramatically reduced the cost of barcodes, thus enabling decentralized deployment across the planet. In this article, we review how DNA barcodes have become a key tool for accelerating biodiversity discovery and analyzing insect communities through both megabarcoding and metabarcoding in an era of insect decline. We predict that DNA barcodes will be particularly important for assembling image training sets for deep learning algorithms, global biodiversity genomics, and functional analysis of insect communities.Review in Advance first posted online on October 1, 2024. Updated on November 5, 2024. Changes may still occur before final publication.
Epigenetic Regulation in Insect-Microbe Interactions
Lai Y and Wang S
Insects have evolved diverse interactions with a variety of microbes, such as pathogenic fungi, bacteria, and viruses. The immune responses of insect hosts, along with the dynamic infection process of microbes in response to the changing host environment and defenses, require rapid and fine-tuned regulation of gene expression programs. Epigenetic mechanisms, including DNA methylation, histone modifications, and noncoding RNA regulation, play important roles in regulating the expression of genes involved in insect immunity and microbial pathogenicity. This review highlights recent discoveries and insights into epigenetic regulatory mechanisms that modulate insect-microbe interactions. A deeper understanding of these regulatory mechanisms underlying insect-microbe interactions holds promise for the development of novel strategies for biological control of insect pests and mitigation of vector-borne diseases.
Venoms of Lepidoptera: Evolution, Composition, and Molecular Modes of Action
Walker AA
Animal venoms are a focus of research due to the hazards they represent and to their relationship to evolution and ecology, pharmacology, biodiscovery, and biotechnology. Venoms have evolved multiple times in Lepidoptera, mostly as defensive adaptations that protect the larval life stages. While venoms are always produced in structures derived from cuticle and setae, they are diverse in their composition and bioactivity, reflecting their multiple evolutionary origins. The most common result of envenomation by lepidopterans is pain and inflammation, but envenomation by some species causes fatal hemorrhagic syndromes or chronic inflammatory conditions in humans or veterinary pathologies such as equine amnionitis and fetal loss. The handful of lepidopteran venom toxins that have been characterized includes coagulotoxins from (Saturniidae) and pain-causing cecropin-like peptides from (Limacodidae). However, our knowledge of lepidopteran venoms remains comparatively poor, with further studies required to yield a clear picture of the evolution, composition, and function of venoms produced by Lepidoptera.
The Role of ()-β-Farnesene in Tritrophic Interactions: Biosynthesis, Chemoreception, and Evolution
Wang B, Jacquin-Joly E and Wang G
()-β-farnesene (EBF) stands out as a crucial volatile organic compound, exerting significant influence on the complex interactions between plants, aphids, and predator insects. Serving as an alarm signal within aphids, EBF is also emitted by plants as a defense mechanism to attract aphid predators. This review delves into EBF sources, functions, biosynthesis, detection mechanisms, and its coevolutionary impacts on aphids and insect predators. The exploration underscores the need to comprehend the biophysical and structural foundations of EBF receptors in aphids, emphasizing their role in unraveling the intricate patterns and mechanisms of interaction between EBF and target receptors. Furthermore, we advocate for adopting structure-based or machine-learning methodologies to anticipate receptor-ligand interactions. On the basis of this knowledge, we propose future research directions aiming at designing, optimizing, and screening more stable and efficient active odorants. A pivotal outcome of this comprehensive investigation aims to contribute to the development of more effective aphid-targeted control strategies.
Harmonizing Multisource Data to Inform Vector-Borne Disease Risk Management Strategies
Lowe R and Codeço CT
In the last few decades, we have witnessed the emergence of new vector-borne diseases (VBDs), the globalization of endemic VBDs, and the urbanization of previously rural VBDs. Data harmonization forms the basis of robust decision-support systems designed to protect at-risk communities from VBD threats. Strong interdisciplinary partnerships, protocols, digital infrastructure, and capacity-building initiatives are essential for facilitating the coproduction of robust multisource data sets. This review provides a foundation for researchers and practitioners embarking on data harmonization efforts to () better understand the links among environmental degradation, climate change, socioeconomic inequalities, and VBD risk; () conduct risk assessments, health impact attribution, and projection studies; and () develop robust early warning and response systems. We draw upon best practices in harmonizing data for two well-studied VBDs, dengue and malaria, and provide recommendations for the evolution of research and digital technology to improve data harmonization for VBD risk management.
Management of Insect Pests on Tea Plantations: Safety, Sustainability, and Efficiency
Chen Z and Luo Z
Tea is the second most consumed beverage after water; thus, tea plants are economically important crops in many countries. The frequent application of chemical pesticides over large plantations of tea monoculture has led to pest outbreaks. In recent years, high amounts of highly water-soluble pesticides have been applied because of the proliferation of piercing-sucking insects; however, this method poses health hazards for humans and has negative environmental effects. This review outlines the effects of pesticide applications on the succession of tea pest populations, the risks posed by the use of highly water-soluble pesticides, and the principles of tea pest management. Various pest control techniques, including physical, biological, chemical-ecological, chemical pesticide, and cultural control methods, have been used in the last few decades. We discuss future prospects and challenges for the integrated pest management of tea plantations.
Complexities in the Implementation and Maintenance of Integrated Pest Management in Potato
Gao Y, Alyokhin A, Prager SM, Reitz S and Huseth A
Integrated pest management (IPM) is an educated and systematic effort to use multiple control techniques to reduce pest damage to economically acceptable levels while minimizing negative environmental impacts. Although its benefits are widely acknowledged, IPM is not universally practiced by farmers. Potato farming, which produces one of the most important staple crops in the world, provides a good illustration of the issues surrounding IPM adoption. Potatoes are attacked by a complex of insect pests that can inflict catastrophic crop losses. Potato production has gone through the processes of consolidation and intensification, which are linked to increased pest problems, particularly selection for insecticide-resistant pest populations. While use of insecticides remains the most common method of pest control in potatoes, other techniques, including crop rotation and natural enemies, are also available. In addition, there are effective monitoring techniques for many potato pests. However, reliable economic thresholds are often lacking. Potato ecosystems are complex and diverse; therefore, the knowledge necessary for developing ecologically based pest management is not easily obtained or transferable. Furthermore, potato systems change with the arrival of new pest species and the evolution of existing pests. Modern technological advances, such as remote sensing and molecular biotechnology, are likely to improve potato IPM. However, these tools are not going to solve all problems. IPM is not just about integrating different techniques; it is also about integrating the efforts and concerns of all stakeholders. The collaboration of farmers and scientists in agricultural research is needed to foster the development of IPM systems that are appropriate for grower implementation and thus more likely to be adopted. Additional emphasis also needs to be placed on the fact that not only does IPM decrease degradation of the environment, but it also improves the economic well-being of its practitioners.
How Insect Exocrine Glands Work
Foster SP and Casas J
Exocrine glands release a secretion to the body surface or into a lumen and are likely to be found in all insect taxa. Their secretions are diverse, serving many physiological, behavioral, and defensive functions. Much research has characterized gland structure and secretion identity and function, but little research has attempted to understand how these glands work to release secretion amounts in a timescale appropriate to function: How are some (e.g., physiological) secretions released in small amounts over long times, while others (e.g., defense) are released in large amounts infrequently? We describe a qualitative model, comprising intracellular, extracellular, and external compartments for secretion storage; rates of movement of secretion from one compartment to the next; physicochemical properties of secretions; and controlling behaviors, which may explain the release dynamics of secretions from these glands. It provides a template for quantitative dynamic studies investigating the operation, control, release, and biomimicry of exocrine glands.
Insect Mitochondrial Genomics: A Decade of Progress
Cameron SL
The past decade has seen the availability of insect genomic data explode, with mitochondrial (mt) genome data seeing the greatest growth. The widespread adoption of next-generation sequencing has solved many earlier methodological limitations, allowing the routine sequencing of whole mt genomes, including from degraded or museum specimens and in parallel to nuclear genomic projects. The diversity of available taxa now allows finer-scale comparisons between mt and nuclear phylogenomic analyses; high levels of congruence have been found for most orders, with some significant exceptions (e.g., Odonata, Mantodea, Diptera). The evolution of mt gene rearrangements and their association with haplodiploidy have been tested with expanded taxonomic sampling, and earlier proposed trends have been largely supported. Multiple model systems have been developed based on findings unique to insects, including mt genome fragmentation (lice and relatives) and control region duplication (thrips), allowing testing of hypothesized evolutionary drivers of these aberrant genomic phenomena. Finally, emerging research topics consider the contributions of mt genomes to insect speciation and habitat adaption, with very broad potential impacts. Integration between insect mt genomic research and other fields within entomology continues to be our field's greatest opportunity and challenge.
Insect Pest Management and Environmental Risk
Peterson RKD
Insect pests and insect pest management tactics impose risks to the environment. Environmental risk assessment is a formalized paradigm for the objective evaluation of risk in which assumptions and uncertainties are clearly presented. Therefore, a better understanding of the environmental risks and especially the comparative risks posed by insect pests and management tactics will improve integrated pest management. Risk assessments for insect pest management tactics are much more common for pesticides and genetically engineered crops than for biological control, cultural control, and semiochemicals. The reasons for this discrepancy include evidence of deleterious effects and data availability for pesticides and genetically engineered crops, public perceptions of tactics, and politics. Regardless of the regulatory oversight and frequency of risk assessments, all tactics should be subject to the risk assessment paradigm to assist in societal decisions.
The Evolution of Queen Pheromone Production and Detection in the Reproductive Division of Labor in Social Insect Colonies
Liebig J and Amsalem E
Structurally diverse queen pheromones and fertility signals regulate the reproductive division of labor of social insects, such as ants, termites, some bees, and some wasps. The independent evolution of sociality in these taxa allows for the exploration of how natural history differences in sender and receiver properties led to the evolution of these complex communication systems. While describing the different effects and the structural diversity of queen pheromones, we identify two major syndromes that mostly separate ants and wasps from bees and termites in their use of different pheromone classes. We compare olfactory receptor evolution among these groups and review physiological and hormonal links to fecundity and pheromone production. We explore the cases in which queen pheromone evolution is conserved, convergent, or parallel and those in which queen pheromone responses are more likely to be learned or innate. More mechanistic information about the pathways linking fecundity to queen pheromone production and perception could help close major knowledge gaps.
Phenotypic Plasticity in Locusts: Trade-Off Between Migration and Reproduction
Guo X and Kang L
Locusts exhibit phenotypic plasticity in response to population density changes, with distinct phenotypes in the solitary and gregarious phases. In the past decade, many studies have revealed the molecular mechanisms underlying phase changes, which include the change of body coloration, pheromones, behavior, flight, fecundity, immunity, and aging. Our understanding of the molecular mechanisms related to these phenotypic differences has expanded in breadth and depth with the decoding of the locust genome, involving transcriptional, post-transcriptional, translational, and epigenetic regulation. Large-scale regulation networks composed of genes and noncoding RNAs reflect the systematic modifications of the locust phase transition in response to environmental changes. Gene manipulation techniques have verified the functions of specific genes and related pathways in phase changes. This review highlights the latest advances in studies of locust phase changes and suggests that the divergence of energy and metabolism allocation in gregarious and solitary locusts is an adaptive strategy for long-distance migration and local reproduction, respectively. Finally, we propose future research directions and discuss emerging questions in the area of phenotypic plasticity of locusts.
The Evolutionary Biology of Chelicerata
Sharma PP and Gavish-Regev E
Chelicerata constitutes an ancient, biodiverse, and ecologically significant group of Arthropoda. The study of chelicerate evolution has undergone a renaissance in the past decade, resulting in major changes to our understanding of the higher-level phylogeny and internal relationships of living orders. Included among these conceptual advances are the discoveries of multiple whole-genome duplication events in a subset of chelicerate orders, such as horseshoe crabs, spiders, and scorpions. As a result, longstanding hypotheses and textbook scenarios of chelicerate evolution, such as the monophyly of Arachnida and a single colonization of land by the common ancestor of arachnids, have come into contention. The retention of ancient, duplicated genes across this lineage also offers fertile ground for investigating the role of gene duplication in chelicerate macroevolution. This new frontier of investigation is paralleled by the timely establishment of the first gene editing protocols for arachnid models, facilitating a new generation of experimental approaches.
Biology, Ecology, and Management of Flea Beetles in Crops
Li Z, Costamagna AC, Beran F and You M
vegetable and oilseed crops are attacked by several different flea beetle species (Chrysomelidae: Alticini). Over the past decades, most research has focused on two species, and , which are major pests of oilseed rape in North America. More recently, and especially after the ban of neonicotinoids in the European Union, the cabbage stem flea beetle, , has become greatly important and is now considered to be the major pest of winter oilseed rape in Europe. The major challenges to flea beetle control are the prediction of population dynamics in the field, differential susceptibility to insecticides, and the lack of resistant plant cultivars and other economically viable alternative management strategies. At the same time, many fundamental aspects of flea beetle biology and ecology, which may be relevant for the development of sustainable control strategies, are not well understood. This review focuses on the interactions between flea beetles and plants and summarizes the literature on current management strategies with an emphasis on the potential for biological control in flea beetle management.
Vector Biology and Integrated Management of Malaria Vectors in China
Zhao T and Xue RD
Malaria is an infectious disease caused by parasites, transmitted by , , , and in China. In 2021, the disease was eliminated in China after more than 70 years of efforts implementing an integrated mosquito management strategy. This strategy comprised indoor residual spray, insecticide-treated bed nets, irrigation management, and rice-fish coculture based on an understanding of taxonomic status and ecological behaviors of vector species, in conjunction with mass drug administration and promotion of public education. However, China still faces postelimination challenges, including the importation of approximately 2,000-4,000 cases of malaria into the country each year, as well as widespread resistance to pyrethroid insecticides in ; these challenges require long-term vector surveillance to understand the distribution, population density, and development of resistance in vector mosquitoes to prevent local epidemics caused by imported malaria cases.
How Nutrients Mediate the Impacts of Global Change on Locust Outbreaks
Cease AJ
Locusts are grasshoppers that can migrate en masse and devastate food security. Plant nutrient content is a key variable influencing population dynamics, but the relationship is not straightforward. For an herbivore, plant quality depends not only on the balance of nutrients and antinutrients in plant tissues, which is influenced by land use and climate change, but also on the nutritional state and demands of the herbivore, as well as its capacity to extract nutrients from host plants. In contrast to the concept of a positive relationship between nitrogen or protein concentration and herbivore performance, a five-decade review of lab and field studies indicates that equating plant N to plant quality is misleading because grasshoppers respond negatively or neutrally to increasing plant N just as often as they respond positively. For locusts specifically, low-N environments are actually beneficial because they supply high energy rates that support migration. Therefore, intensive land use, such as continuous grazing or cropping, and elevated ambient CO levels that decrease the protein:carbohydrate ratios of plants are predicted to broadly promote locust outbreaks.
Taxonomy, Biology, Symbionts, Omics, and Management of Palm Weevils (Coleoptera: Curculionidae: Dryophthorinae)
Hoddle MS, Antony B, El-Shafie HAF, Chamorro ML, Milosavljević I, Löhr B and Faleiro JR
Palm weevils, spp., are destructive pests of native, ornamental, and agricultural palm species. Of the 10 recognized species, two of the most injurious species, and , both of which have spread beyond their native range, are the best studied. Due to its greater global spread and damage to edible date industries in the Middle East, has received more research interest. Integrated pest management programs utilize traps baited with aggregation pheromone, removal of infested palms, and insecticides. However, weevil control is costly, development of resistance to insecticides is problematic, and program efficacy can be impaired because early detection of infestations is difficult. The genome of has been sequenced, and omics research is providing insight into pheromone communication and changes in volatile and metabolism profiles of weevil-infested palms. We outline how such developments could lead to new control strategies and early detection tools.