Annual Review of Entomology - Volume 66, 2021

This review was solicited as an autobiography. The “problems” in my title have two meanings. First, they were professional difficulties caused by my decision to study oviposition preferences of butterflies that were not susceptible to traditional preference-testing designs. Until I provided video, my claim that the butterflies duplicate natural post-alighting host-assessment behavior when placed on hosts by hand was not credible, and the preference-testing technique that I had developed elicited skepticism, anger, and derision. The second meaning of “problems” is scientific. Insect preference comes with complex dimensionality that interacts with host acceptability. Part Two of this review describes how my group's work in this area has revealed unexpected axes of variation in plant–insect interactions—axes capable of frustrating attempts to derive unequivocal conclusions from apparently sensible experimental designs. The possibility that these complexities are lurking should be kept in mind as preference and performance experiments are devised.

Termites have long been studied for their symbiotic associations with gut microbes. In the late nineteenth century, this relationship was poorly understood and captured the interest of parasitologists such as Joseph Leidy; this research led to that of twentieth-century biologists and entomologists including Cleveland, Hungate, Trager, and Lüscher. Early insights came via microscopy, organismal, and defaunation studies, which led to descriptions of microbes present, descriptions of the roles of symbionts in lignocellulose digestion, and early insights into energy gas utilization by the host termite. Focus then progressed to culture-dependent microbiology and biochemical studies of host–symbiont complementarity, which revealed specific microhabitat requirements for symbionts and noncellulosic mechanisms of symbiosis (e.g., N2 fixation). Today, knowledge on termite symbiosis has accrued exponentially thanks to omic technologies that reveal symbiont identities, functions, and interdependence, as well as intricacies of host–symbiont complementarity. Moving forward, the merging of classical twentieth-century approaches with evolving omic tools should provide even deeper insights into host–symbiont interplay.

Insect cuticular hydrocarbons (CHCs) consist of complex mixtures of straight-chain alkanes and alkenes, and methyl-branched hydrocarbons. In addition to restricting water loss through the cuticle and preventing desiccation, they have secondarily evolved to serve a variety of functions in chemical communication and play critical roles as signals mediating the life histories of insects. In this review, we describe the physical properties of CHCs that allow for both waterproofing and signaling functions, summarize their roles as inter- and intraspecific chemical signals, and discuss the influences of diet and environment on CHC profiles. We also present advances in our understanding of hydrocarbon biosynthesis. Hydrocarbons are biosynthesized in oenocytes and transported to the cuticle by lipophorin proteins. Recent work on the synthesis of fatty acids and their ultimate reductive decarbonylation to hydrocarbons has taken advantage of powerful new tools of molecular biology, including genomics and RNA interference knockdown of specific genes, to provide new insights into the biosynthesis of hydrocarbons.

As an overarching immune mechanism, RNA interference (RNAi) displays pathogen specificity and memory via different pathways. The small interfering RNA (siRNA) pathway is the primary antiviral defense mechanism against RNA viruses of insects and plays a lesser role in defense against DNA viruses. Reflecting the pivotal role of the siRNA pathway in virus selection, different virus families have independently evolved unique strategies to counter this host response, including protein-mediated, decoy RNA–based, and microRNA-based strategies. In this review, we outline the interplay between insect viruses and the different pathways of the RNAi antiviral response; describe practical application of these interactions for improved expression systems and for pest and disease management; and highlight research avenues for advancement of the field.

All organisms are exposed to changes in their environment throughout their life cycle. When confronted with these changes, they adjust their development and physiology to ensure that they can produce the functional structures necessary for survival and reproduction. While some traits are remarkably invariant, or robust, across environmental conditions, others show high degrees of variation, known as plasticity. Generally, developmental processes that establish cell identity are thought to be robust to environmental perturbation, while those relating to body and organ growth show greater degrees of plasticity. However, examples of plastic patterning and robust organ growth demonstrate that this is not a hard-and-fast rule.In this review, we explore how the developmental context and the gene regulatory mechanisms underlying trait formation determine the impacts of the environment on development in insects. Furthermore, we outline future issues that need to be resolved to understand how the structure of signaling networks defines whether a trait displays plasticity or robustness.

Thrips (Thysanoptera) are small insects that can cause huge problems in agriculture, horticulture, and forestry through feeding and the transmission of plant viruses. They produce a rich chemical diversity of pheromones and allomones and also respond to a broad range of semiochemicals from plants. These semiochemicals offer many opportunities to develop new approaches to pest management. Aggregation pheromones and plant-derived semiochemicals are already available in commercial products. We review these semiochemicals and consider how we can move away from using them mainly for monitoring to using them for control. We still know very little about the behavioral responses of thrips to semiochemicals, and we show that research in this area is needed to improve the use of semiochemicals in pest management. We also propose that thrips should be used as a model system for semiochemically mediated behaviors of small insects that have limited ability to fly upwind.

Insecticidal proteins from the bacterium Bacillus thuringiensis (Bt) are used in sprayable formulations or produced in transgenic crops as the most successful alternatives to synthetic pesticides. The most relevant threat to sustainability of Bt insecticidal proteins (toxins) is the evolution of resistance in target pests. To date, high-level resistance to Bt sprays has been limited to one species in the field and another in commercial greenhouses. In contrast, there are currently seven lepidopteran and one coleopteran species that have evolved practical resistance to transgenic plants producing insecticidal Bt proteins. In this article, we present a review of the current knowledge on mechanisms of resistance to Bt toxins, with emphasis on key resistance genes and field-evolved resistance, to support improvement of Bt technology and its sustainability.

Legume pod borer, Maruca vitrata, has emerged as a major pest on food legumes in Asia and Africa. It is an oligophagous pest, feeding on over 70 species in Fabaceae. We examine the species complex in Asia, Africa, Oceania, and the Americas, with an emphasis on molecular taxonomy. Studies on pheromone production and perception suggest the existence of pheromone polymorphism, especially in Asia and Africa. No Maruca-resistant varieties are available in the major food legumes including cowpea, pigeonpea, mungbean, and yard-long bean. Legume growers use chemical pesticides indiscriminately, leading to the development of pesticide resistance. However recent developments in habitat management, classical biocontrol with more efficient parasitoids, biopesticides, and judicious use of insecticides pave the way for sustainable management of M. vitrata, which can reduce the pesticide misuse. Active engagement of the private sector and policy makers can increase the adoption of integrated pest management approaches in food legumes.

Global change includes a substantial increase in the frequency and intensity of extreme high temperatures (EHTs), which influence insects at almost all levels. The number of studies showing the ecological importance of EHTs has risen in recent years, but the knowledge is rather dispersed in the contemporary literature. In this article, we review the biological and ecological effects of EHTs actually experienced in the field, i.e., when coupled to fluctuating thermal regimes. First, we characterize EHTs in the field. Then, we summarize the impacts of EHTs on insects at various levels and the processes allowing insects to buffer EHTs. Finally, we argue that the mechanisms leading to positive or negative impacts of EHTs on insects can only be resolved from integrative approaches considering natural thermal regimes. Thermal extremes, perhaps more than the gradual increase in mean temperature, drive insect responses to climate change, with crucial impacts on pest management and biodiversity conservation.

Although nectar is consumed, primarily as a supplemental food, by a broad range of insects spanning at least five orders, it is processed and stored by only a small number of species, most of which are bees and wasps in the superfamily Apoidea. Within this group, Apis mellifera has evolved remarkable adaptations facilitating nectar processing and storage; in doing so, this species utilizes the end product, honey, for diverse functions with few if any equivalents in other phytophagous insects. Honey and its phytochemical constituents, some of which likely derive from propolis, have functional significance in protecting honey bees against microbial pathogens, toxins, and cold stress, as well as in regulating development and adult longevity. The distinctive properties of A. mellifera honey appear to have arisen in multiple ways, including genome modification; partnerships with microbial symbionts; and evolution of specialized behaviors, including foraging for substances other than nectar. That honey making by A. mellifera involves incorporation of exogenous material other than nectar, as well as endogenous products such as antimicrobial peptides and royal jelly, suggests that regarding honey as little more than a source of carbohydrates for bees is a concept in need of revision.

In the past 25 years, studies on interactions between chewing lice and their bird hosts have increased notably. This body of work reveals that sampling of live avian hosts, collection of the lice, and the aggregated distributions of louse infestations pose challenges for assessing louse populations. The number of lice on a bird varies among host taxa, often with host size and social system. Host preening behavior limits louse abundance, depending on bill shape. The small communities of lice (typically one–four species) that live on individual birds show species-specific patterns of abundance, with consistently common and rare species, and lower year-to-year population variability than other groups of insects. Most species of lice appear to breed continuously on their hosts, with seasonal patterns of abundance sometimes related to host reproduction and molting. Competition may have led to spatial partitioning of the host by louse species, but seldom contributes to current patterns of abundance.

Spiders (Araneae) make up a remarkably diverse lineage of predators that have successfully colonized most terrestrial ecosystems. All spiders produce silk, and many species use it to build capture webs with an extraordinary diversity of forms. Spider diversity is distributed in a highly uneven fashion across lineages. This strong imbalance in species richness has led to several causal hypotheses, such as codiversification with insects, key innovations in silk structure and web architecture, and loss of foraging webs. Recent advances in spider phylogenetics have allowed testing of some of these hypotheses, but results are often contradictory, highlighting the need to consider additional drivers of spider diversification. The spatial and historical patterns of diversity and diversification remain contentious. Comparative analyses of spider diversification will advance only if we continue to make progress with studies of species diversity, distribution, and phenotypic traits, together with finer-scale phylogenies and genomic data.

Distant and predictable features in the environment make ideal compass cues to allow movement along a straight path. Ball-rolling dung beetles use a wide range of different signals in the day or night sky to steer themselves along a fixed bearing. These include the sun, the Milky Way, and the polarization pattern generated by the moon. Almost two decades of research into these remarkable creatures have shown that the dung beetle's compass is flexible and readily adapts to the cues available in its current surroundings. In the morning and afternoon, dung beetles use the sun to orient, but at midday, they prefer to use the wind, and at night or in a forest, they rely primarily on polarized skylight to maintain straight paths. We are just starting to understand the neuronal substrate underlying the dung beetle's compass and the mystery of why these beetles start each journey with a dance.

Arthropod–fungus interactions involving the Laboulbeniomycetes have been pondered for several hundred years. Early studies of Laboulbeniomycetes faced several uncertainties. Were they parasitic worms, red algal relatives, or fungi? If they were fungi, to which group did they belong? What was the nature of their interactions with their arthropod hosts? The historical misperceptions resulted from the extraordinary morphological features of these oddly constructed ectoparasitic fungi. More recently, molecular phylogenetic studies, in combination with a better understanding of life histories, have clearly placed these fungi among filamentous Ascomycota (subphylum Pezizomycotina). Species discovery and research on the classification of the group continue today as arthropods, and especially insects, are routinely collected and examined for the presence of Laboulbeniomycetes. Newly armed with molecular methods, mycologists are poisedto use Laboulbeniomycetes–insect associations as models for the study of a variety of basic evolutionary and ecological questions involving host–parasite relationships, modes of nutrient intake, population biology, host specificity, biological control, and invasion biology. Collaboration between mycologists and entomologists is essential to successfully advance knowledge of Laboulbeniomycetes and their intimate association with their hosts.

Ecological research conducted over the past five decades has shown that increasing tree species richness at forest stands can improve tree resistance to insect pest damage. However, the commonality of this finding is still under debate. In this review, we provide a quantitative assessment (i.e., a meta-analysis) of tree diversity effects on insect herbivory and discuss plausible mechanisms underlying the observed patterns. We provide recommendations and working hypotheses that can serve to lay the groundwork for research to come. Based on more than 600 study cases, our quantitative review indicates that insect herbivory was, on average, lower in mixed forest stands than in pure stands, but these diversity effects were contingent on herbivore diet breadth and tree species composition. In particular, tree species diversity mainly reduced damage of specialist insect herbivores in mixed stands with phylogenetically distant tree species. Overall, our findings provide essential guidance for forest pest management.

Feeding on living or dead plant material is widespread in insects. Seminal work on termites and aphids has provided profound insights into the critical nutritional role that microbes play in plant-feeding insects. Some ants, beetles, and termites, among others, have evolved the ability to use microbes to gain indirect access to plant substrate through the farming of a fungus on which they feed. Recent genomic studies, including studies of insect hosts and fungal and bacterial symbionts, as well as metagenomics and proteomics, have provided important insights into plant biomass digestion across insect–fungal mutualisms. Not only do advances in understanding of the divergent and complementary functions of complex symbionts reveal the mechanism of how these herbivorous insects catabolize plant biomass, but these symbionts also represent a promising reservoir for novel carbohydrate-active enzyme discovery, which is of considerable biotechnological interest.

Many insects locate resources such as a mate, a host, or food by flying upwind along the odor plumes that these resources emit to their source. A windborne plume has a turbulent structure comprised of odor filaments interspersed with clean air. As it propagates downwind, the plume becomes more dispersed and dilute, but filaments with concentrations above the threshold required to elicit a behavioral response from receiving organisms can persist for long distances. Flying insects orient along plumes by steering upwind, triggered by the optomotor reaction. Sequential measurements of differences in odor concentration are unreliable indicators of distance to or direction of the odor source. Plume intermittency and the plume's fine-scale structure can play a role in setting an insect's upwind course. The prowess of insects in navigating to odor sources has spawned bioinspired virtual models and even odor-seeking robots, although some of these approaches use mechanisms that are unnecessarily complex and probably exceed an insect's processing capabilities.

During the past 20 years, more than 1,600 species of well-preserved fossil insects, including members of over 270 families within 24 orders, have been described from the Middle Jurassic Yanliao Entomofauna and Early Cretaceous Jehol Entomofauna in Northeastern China. Diversified fossil insects not only document the origin, systematics, and early evolution of many lineages, but also reveal these lineages’ behaviors and interactions with coexisting plants, vertebrates, and other insects in their ecosystems. Fossil evidence has been documented, for example, regarding insects’ feeding and pollination mutualism with gymnosperms; ectoparasitic feeding on blood of vertebrates; camouflage, mimicry of gymnosperm plants, and eyespot warning; sound stridulation for attracting potential mates; and sexual display, mating, egg-laying, and parental care. In this article, we review the diverse taxonomy of mid-Mesozoic insects of Northeastern China and elucidate their behaviors and interactions within their ecosystems, which have impacted their early evolution and development into extant insects.

Insects are major contributors to our understanding of the interaction between transposable elements (TEs) and their hosts, owing to seminal discoveries, as well as to the growing number of sequenced insect genomes and population genomics and functional studies. Insect TE landscapes are highly variable both within and across insect orders, although phylogenetic relatedness appears to correlate with similarity in insect TE content. This correlation is unlikely to be solely due to inheritance of TEs from shared ancestors and may partly reflect preferential horizontal transfer of TEs between closely related species. The influence of insect traits on TE landscapes, however, remains unclear. Recent findings indicate that, in addition to being involved in insect adaptations and aging, TEs are seemingly at the cornerstone of insect antiviral immunity. Thus, TEs are emerging as essential insect symbionts that may have deleterious or beneficial consequences on their hosts, depending on context.

Ticks exist on all continents and carry more zoonotic pathogens than any other type of vector. Ticks spend most of their lives in the external environment away from the host and are thus expected to be affected by changes in climate. Most empirical and theoretical studies demonstrate or predict range shifts or increases in ticks and tick-borne diseases, but there can be a lot of heterogeneity in such predictions. Tick-borne disease systems are complex, and determining whether changes are due to climate change or other drivers can be difficult. Modeling studies can help tease apart and understand the roles of different drivers of change. Predictive models can also be invaluable in projecting changes according to different climate change scenarios. However, validating these models remains challenging, and estimating uncertainty in predictions is essential. Another focus for future research should be assessing the resilience of ticks and tick-borne pathogens to climate change.

Of the approximately 1,200 plant virus species that have been described to date, nearly one-third are single-stranded DNA (ssDNA) viruses, and all are transmitted by insect vectors. However, most studies of vector transmission of plant viruses have focused on RNA viruses. All known plant ssDNA viruses belong to two economically important families, Geminiviridae and Nanoviridae, and in recent years, there have been increased efforts to understand whether they have evolved similar relationships with their respective insect vectors. This review describes the current understanding of ssDNA virus–vector interactions, including how these viruses cross insect vector cellular barriers, the responses of vectors to virus circulation, the possible existence of viral replication within insect vectors, and the three-way virus–vector–plant interactions. Despite recent breakthroughs in our understanding of these viruses, many aspects of plant ssDNA virus transmission remain elusive. More effort is needed to identify insect proteins that mediate the transmission of plant ssDNA viruses and to understand the complex virus–insect–plant three-way interactions in the field during natural infection.

Insects play important roles as predators, prey, pollinators, recyclers, hosts, parasitoids, and sources of economically important products. They can also destroy crops; wound animals; and serve as vectors for plant, animal, and human diseases. Gene drive—a process by which genes, gene complexes, or chromosomes encoding specific traits are made to spread through wild populations, even if these traits result in a fitness cost to carriers—provides new opportunities for altering populations to benefit humanity and the environment in ways that are species specific and sustainable. Gene drive can be used to alter the genetic composition of an existing population, referred to as population modification or replacement, or to bring about population suppression or elimination. We describe technologies under consideration, progress that has been made, and remaining technological hurdles, particularly with respect to evolutionary stability and our ability to control the spread and ultimate fate of genes introduced into populations.

Color vision is widespread among insects but varies among species, depending on the spectral sensitivities and interplay of the participating photoreceptors. The spectral sensitivity of a photoreceptor is principally determined by the absorption spectrum of the expressed visual pigment, but it can be modified by various optical and electrophysiological factors. For example, screening and filtering pigments, rhabdom waveguide properties, retinal structure, and neural processing all influence the perceived color signal. We review the diversity in compound eye structure, visual pigments, photoreceptor physiology, and visual ecology of insects. Based on an overview of the current information about the spectral sensitivities of insect photoreceptors, covering 221 species in 13 insect orders, we discuss the evolution of color vision and highlight present knowledge gaps and promising future research directions in the field.

Trichogramma species make up one of the most commonly used groups of natural enemies for biological control programs worldwide. Given the major successes in using Trichogramma to control economically important lepidopterous pests on agricultural crops in China, the biology and ecology of these wasps have been intensively studied to identify traits that contribute to successful biological control. Since the 1960s, improved mass production of Trichogramma and better augmentative release methods to suppress agricultural pests have been achieved. We review the history of research and development; current knowledge on biodiversity and bio-ecology of the species used; and achievements in mass-rearing methods, release strategies, and current large-scale applications in China. In addition, we discuss potential issues and challenges for Trichogramma research and applications in the future.

Over the past decade, laboratory courses have made a fundamental shift to inquiry-based modules and authentic research experiences. In many cases, these research experiences emphasize addressing novel research questions. Insects are ideal for inquiry-based undergraduate laboratory courses because research on insects is not limited by regulatory, economic, and logistical constraints to the same degree as research on vertebrates. While novel research questions could be pursued with model insect species (e.g., Drosophila, Tribolium), the opportunities presented by non-model insects are much greater, as less is known about non-model species. We review the literature on the use of non-model insect species in laboratory education to provide a resource for faculty interested in developing new authentic inquiry-based laboratory modules using insects. Broader use of insects in undergraduate laboratory education will support the pedagogical goals of increased inquiry and resesarch experiences while at the same time fostering increased interest and research in entomology.