Annual Review of Entomology - Volume 64, 2019

Elizabeth A. Bernays grew up in Australia and studied at the University of Queensland before traveling in Europe and teaching high school in London. She later obtained a PhD in entomology at London University. Then, as a British government scientist, she worked in England and in developing countries on a variety of projects concerned with feeding by herbivorous insects and their physiology and behavior. In 1983, she was appointed professor at the University of California, Berkeley, where her research expanded to a variety of topics, all related to the physiology, behavior, and ecology of feeding in insects. She was awarded a DSc from the University of London, and at about the same time became head of the Department of Entomology and regents’ professor at the University of Arizona. In Arizona, most of her research involved multiple approaches to the understanding of diet breadth in a variety of phytophagous insect species.

Locusts and grasshoppers (Orthoptera: Acridoidea) are among the most dangerous agricultural pests. Their control is critical to food security worldwide and often requires governmental or international involvement. Although locust and grasshopper outbreaks are now better controlled and often shorter in duration and reduced in extent, large outbreaks, often promoted by climate change, continue to occur in many parts of the world. While some locust and grasshopper control systems are still curative, the recognition of the damage these pests can cause and the socioeconomic consequences of locust and grasshopper outbreaks have led to an increasing paradigm shift from crop protection to preventive management. Effective preventive management strategy relies on an improved knowledge of the pest biology and ecology and more efficient monitoring and control techniques.

Nest choice in Temnothorax spp.; task allocation and the regulation of activity in Pheidole dentata, Pogonomyrmex barbatus, and Atta spp.; and trail networks in Monomorium pharaonis and Cephalotes goniodontus all provide examples of correspondences between the dynamics of the environment and the dynamics of collective behavior. Some important aspects of the dynamics of the environment include stability, the threat of rupture or disturbance, the ratio of inflow and outflow of resources or energy, and the distribution of resources. These correspond to the dynamics of collective behavior, including the extent of amplification, how feedback instigates and inhibits activity, and the extent to which the interactions that provide the information to regulate behavior are local or spatially centralized.

Three species of Vespula have become invasive in Australia, Hawai‘i, New Zealand, and North and South America and continue to spread. These social wasp species can achieve high nest densities, and their behavioral plasticity has led to substantial impacts on recipient communities. Ecologically, they affect all trophic levels, restructuring communities and altering resource flows. Economically, their main negative effect is associated with pollination and the apicultural industry. Climate change is likely to exacerbate their impacts in many regions. Introduced Vespula spp. likely experience some degree of enemy release from predators or parasites, although they are exposed to a wide range of microbial pathogens in both their native and introduced range. Toxic baits have been significantly improved over the last decade, enabling effective landscape-level control. Although investigated extensively, no effective biological control agents have yet been found. Emerging technologies such as gene drives are under consideration.

Aphid invasions of North American cereal crops generally have started with colonization of a new region or crop, followed by range expansion and outbreaks that vary in frequency and scale owing to geographically variable influences. To improve understanding of this process and management, we compare the invasion ecology of and management response to three cereal aphids: sugarcane aphid, Russian wheat aphid, and greenbug. The region exploited is determined primarily by climate and host plant availability. Once an area is permanently or annually colonized, outbreak intensity is also affected by natural enemies and managed inputs, such as aphid-resistant cultivars and insecticides. Over time, increases in natural enemy abundance and diversity, improved compatibility among management tactics, and limited threshold-based insecticide use have likely increased resilience of aphid regulation. Application of pest management foundational practices followed by a focus on compatible strategies are relevant worldwide. Area-wide pest management is most appropriate to large-scale cereal production systems, as exemplified in the Great Plains of North America.

Blueberry is a crop native to North America with expanding production and consumption worldwide. In the historical regions of production, integrated pest management (IPM) programs have been developed and provided effective control of key insect pests. These have integrated monitoring programs with physical, cultural, biological, behavioral, and chemical controls to meet the intense demands of consumers and modern food systems. Globalization of the blueberry industry has resulted in new pest-crop associations and the introduction of invasive pests into existing and new blueberry-growing areas. Invasive pests—in particular spotted wing drosophila—have been highly disruptive to traditional IPM programs, resulting in increased use of insecticides and the potential to disrupt beneficial insects. Moreover, regulatory agencies have reduced the number of broad-spectrum insecticides available to growers while facilitating registration and adoption of reduced-risk insecticides that have a narrower spectrum of activity. Despite these new tools, increasing international trade has constrained insecticide use because of maximum residue limits, which are often not standardized across countries. Great potential remains for biological, behavioral, cultural, and physical methods to contribute to blueberry IPM, and with more regions investing in blueberry research, we expect regionally relevant IPM programs to develop in the new production regions.

The objective of bait application envisioned by early researchers was to eliminate the source of infestation, the colony, but because of the lack of adequate evaluation tools, results of field trials with mirex baits in the 1960s were mostly inconclusive. On-the-ground monitoring stations and mark-recapture protocol developed in the 1970s marked the turning point in the field studies of termite baits. Results of field studies with metabolic inhibitors and chitin synthesis inhibitors (CSIs) in the 1990s indicated that a bait toxicant has to be slow-acting and nonrepellent, and its lethal time has to be dose independent. A recent discovery that termites return to the central nest to molt and CSI-poisoned termites die near the royal pair further explains the success of CSI baits in eliminating colonies. Owing to the availability of durable baits that require less-frequent site inspection, more termite control professionals have adopted baiting systems in recent years.

The khapra beetle, Trogoderma granarium, is a voracious feeder of stored products and is considered one of the most important quarantine pests globally. Its ability to survive for long periods under extreme conditions facilitates its spread through international commerce, which has led to invasions of new geographic regions. The khapra beetle is an important quarantine pest for many countries, including the major wheat-producing countries the United States, Canada, Russia, and Australia, and has been classified as one of the 100 worst invasive species worldwide. This species cannot always be controlled by insecticides and other nonchemical methods that are usually effective against other pests of stored products, particularly owing to its diapausing late larval stage. It can rapidly develop at elevated temperatures and under dry conditions, which are not favorable for many major stored-product insects. We synthesize key published work to draw attention to advances in biology, detection and control of the khapra beetle, and directions to consider for future research.

Babesiosis, caused by piroplasmid protozoans in the genus Babesia, is arguably the most important vector-borne disease of livestock and companion animals and is growing in importance as a zoonosis. Ixodid ticks were identified as vectors more than a hundred years ago, but the particular tick species transmitting some significant pathogens are still unknown. Moreover, it is only recently that the complexity of the pathogen–tick relationship has been revealed as a result of studies enabled by gene expression and RNA interference methodology. In this article, we provide details of demonstrated and incriminated vectors, maps of the current knowledge of vector distribution, a summary of established features of the pathogen life cycle in the vector, and an outline of molecular research on pathogen–tick relationships. The article concludes with a discussion of vector ecology and disease epidemiology in a global-change context and with suggestions for future research.

The number of insect species at risk of population decline and extinction is increasing rapidly. Yet we know almost nothing about the ecology of these species, except for at-risk butterflies. A growing body of literature shows how butterfly vital rates, including demography and movement, are essential for guiding conservation and recovery. History has shown us that without these data, conservation decisions often weaken, rather than enhance, population viability. This is especially true in changing landscapes. We review knowledge of vital rates across all at-risk butterflies. We have information on movement for 17 of 283 butterfly species and information on demography for 19 species. We find that habitat-specific movement behavior is key to understanding how to connect populations, and habitat-specific demography is central to managing habitats. Methods and analyses worked out for butterflies can provide a scaffold around which to build studies for the conservation of other at-risk insects.

Epigenetic inheritance is fundamentally important to cellular differentiation and developmental plasticity. In this review, we provide an introduction to the field of molecular epigenetics in insects. Epigenetic information is passed across cell divisions through the methylation of DNA, the modification of histone proteins, and the activity of noncoding RNAs. Much of our knowledge of insect epigenetics has been gleaned from a few model species. However, more studies of epigenetic information in traditionally nonmodel taxa will help advance our understanding of the developmental and evolutionary significance of epigenetic inheritance in insects. To this end, we also provide a brief overview of techniques for profiling and perturbing individual facets of the epigenome. Doing so in diverse cellular, developmental, and taxonomic contexts will collectively help shed new light on how genome regulation results in the generation of diversity in insect form and function.

Bees—including solitary, social, wild, and managed species—are key pollinators of flowering plant species, including nearly three-quarters of global food crops. Their ecological importance, coupled with increased annual losses of managed honey bees and declines in populations of key wild species, has focused attention on the factors that adversely affect bee health, including viral pathogens. Genomic approaches have dramatically expanded understanding of the diversity of viruses that infect bees, the complexity of their transmission routes—including intergenus transmission—and the diversity of strategies bees have evolved to combat virus infections, with RNA-mediated responses playing a prominent role. Moreover, the impacts of viruses on their hosts are exacerbated by the other major stressors bee populations face, including parasites, poor nutrition, and exposure to chemicals. Unraveling the complex relationships between viruses and their bee hosts will lead to improved understanding of viral ecology and management strategies that support better bee health.

The evolutionary origins of the three major families of chemoreceptors in arthropods—the odorant receptor (OR), gustatory receptor (GR), and ionotropic receptor (IR) families—occurred at the base of the Insecta, Animalia, and Protostomia, respectively. Comparison of receptor family sizes across arthropods reveals a generally positive correlation with their widely disparate complexity of chemical ecology. Closely related species reveal the ongoing processes of gene family evolution, including gene duplication, divergence, pseudogenization, and loss, that mediate these larger patterns. Sets of paralogous receptors within species reveal positive selection on amino acids in regions likely to contribute to ligand binding and specificity. Ligands of many ORs and some GRs and IRs have been identified; however, ligand identification for many more chemoreceptors is needed, as are structures for the OR/GR superfamily, to improve our understanding of the molecular evolution of these ecologically important receptors in arthropods.

The voltage-sensitive sodium channel (VSSC) is a critical component of the insect nervous system. Pyrethroids and DDT are insecticides that have been widely used, and they kill insects by perturbations of the VSSC. Decades of insecticide use selected for mutations in Vssc that give rise to resistance in almost all pest insects. However, the mutations responsible for the resistance are not always the same, and some unusual patterns have emerged. This review focuses on what pyrethroid/DDT selection has done, in terms of Vssc changes that have occurred, using four well-studied species as examples of the differences that have evolved. Information is provided about the mutations that occur, potential pathways by which alleles with multiple mutations arose, the relative fitness of the alleles, the levels of resistance conferred, and the geographic distribution of the mutations. The lessons learned and exciting new areas of research are discussed.

The main modes of action of insect parasitoids are considered to be killing their hosts with egg laying followed by offspring development (reproductive mortality), and adults feeding on hosts directly (host feeding). However, parasitoids can also negatively affect their hosts in ways that do not contribute to current or future parasitoid reproduction (nonreproductive effects). Outcomes of nonreproductive effects for hosts can include death, altered behavior, altered reproduction, and altered development. On the basis of these outcomes and the variety of associated mechanisms, we categorize nonreproductive effects into (a) nonconsumptive effects, (b) mutilation, (c) pseudoparasitism, (d) immune defense costs, and (e) aborted parasitism. These effects are widespread and can cause greater impacts on host populations than successful parasitism or host feeding. Nonreproductive effects constitute a hidden dimension of host–parasitoid trophic networks, with theoretical implications for community ecology as well as applied importance for the evaluation of ecosystem services provided by parasitoid biological control agents.

The recent introduction and spread of Helicoverpa armigera throughout South America highlight the invasiveness and adaptability of moths in the Helicoverpa genus. Long-range movement in three key members, H. armigera, H. zea, and H. punctigera, occurs by migration and international trade. These movements facilitate high population admixture and genetic diversity, with important economic, biosecurity, and control implications in today's agricultural landscape. This is particularly true for the spread of resistance alleles to transgenic crops expressing Bacillus thuringiensis (Bt) toxins that are planted over vast areas to suppress Helicoverpa spp. The ability to track long-distance movement through radar technology, population genetic markers, and/or long-distance dispersal modeling has advanced in recent years, yet we still know relatively little about the population trajectories or migratory routes in Helicoverpa spp. Here, we consider how experimental and theoretical approaches can be integrated to fill key knowledge gaps and assist management practices.

Many insects are capable of developing into either long-winged or short-winged (or wingless) morphs, which enables them to rapidly match heterogeneous environments. Thus, the wing polymorphism is an adaptation at the root of their ecological success. Wing polymorphism is orchestrated at various levels, starting with the insect's perception of environmental cues, then signal transduction and signal execution, and ultimately the transmitting of signals into physiological adaption in accordance with the particular morph produced. Juvenile hormone and ecdysteroid pathways have long been proposed to regulate wing polymorphism in insects, but rigorous experimental evidence is lacking. The breakthrough findings of ecdysone receptor regulation on transgenerational wing dimorphism in the aphid Acyrthosiphon pisum and of insulin signaling in the planthopper Nilaparvata lugens greatly broaden our understanding of wing polymorphism at the molecular level. Recently, the advent of high-throughput sequencing coupled with functional genomics provides powerful genetic tools for future insights into the molecular bases underlying wing polymorphism in insects.

The insect fat body is analogous to vertebrate adipose tissue and liver. In this review, the new and exciting advancements made in fat body biology in the last decade are summarized. Controlled by hormonal and nutritional signals, insect fat body cells undergo mitosis during embryogenesis, endoreplication during the larval stages, and remodeling during metamorphosis and regulate reproduction in adults. Fat body tissues are major sites for nutrient storage, energy metabolism, innate immunity, and detoxification. Recent studies have revealed that the fat body plays a central role in the integration of hormonal and nutritional signals to regulate larval growth, body size, circadian clock, pupal diapause, longevity, feeding behavior, and courtship behavior, partially by releasing fat body signals to remotely control the brain. In addition, the fat body has emerged as a fascinating model for studying metabolic disorders and immune diseases. Potential future directions for fat body biology are also proposed herein.

The parasitoid wasp family Braconidae is likely the second-most species-rich family in the animal kingdom. Braconid wasps are widely distributed and often encountered. They constitute one of the principal groups of natural enemies of phytophagous insects, of which many are serious pest species. The enormous biological diversification of braconid wasps has led to many homoplasies, which contributed widely to instabilities in historical classifications. Recent studies using combinations of genetic markers or total mitochondrial genomes allow for better founded groupings and will ultimately lead to a stable classification. We present the current status of the phylogenetics of the Braconidae in a historical perspective and our understanding of the effects on higher classification.