Annual Review of Entomology - Volume 65, 2020

This autobiographical article describes the research career of Lynn M. Riddiford from its early beginnings in a summer program for high school students at Jackson Laboratory to the present “retirement” at the Friday Harbor Laboratories. The emphasis is on her forays into many areas of insect endocrinology, supported by her graduate students and postdoctoral associates. The main theme is the hormonal regulation of metamorphosis, especially the roles of juvenile hormone (JH). The article describes the work of her laboratory first in the elucidation of the endocrinology of the tobacco hornworm, Manduca sexta, and later in the molecular aspects of the regulation of cuticular and pigment proteins and of the ecdysone-induced transcription factor cascade during molting and metamorphosis. Later studies utilized Drosophila melanogaster to answer further questions about the actions of JH.

Western flower thrips, Frankliniella occidentalis, first arose as an important invasive pest of many crops during the 1970s–1980s. The tremendous growth in international agricultural trade that developed then fostered the invasiveness of western flower thrips. We examine current knowledge regarding the biology of western flower thrips, with an emphasis on characteristics that contribute to its invasiveness and pest status. Efforts to control this pest and the tospoviruses that it vectors with intensive insecticide applications have been unsuccessful and have created significant problems because of the development of resistance to numerous insecticides and associated outbreaks of secondary pests. We synthesize information on effective integrated management approaches for western flower thrips that have developed through research on its biology, behavior, and ecology. We further highlight emerging topics regarding the species status of western flower thrips, as well as its genetics, biology, and ecology that facilitate its use as a model study organism and will guide development of appropriate management practices.

Nest site availability and quality are important for maintaining robust populations and communities of wild bees. However, for most species, nesting traits and nest site conditions are poorly known, limiting both our understanding of basic ecology for bee species and conservation efforts. Additionally, many of the threats commonly associated with reducing bee populations have effects that can extend into nests but are largely unstudied. In general, threats such as habitat disturbances and climate change likely affect nest site availability and nest site conditions, which in turn affect nest initiation, growth, development, and overwintering success of bees. To facilitate a better understanding of how these and other threats may affect nesting bees, in this review, I quantify key nesting traits and environmental conditions and then consider how these traits may intersect with observed and anticipated changes in nesting conditions experienced by wild bees. These data suggest that the effects of common threats to bees through nesting may strongly influence their survival and persistence but are vastly understudied. Increasing research into nesting biology and incorporating nesting information into conservation efforts may help improve conservation of this declining but critical group.

Sexual size dimorphism is one of the most striking animal traits, and among terrestrial animals, it is most extreme in certain spider lineages. The most extreme sexual size dimorphism (eSSD) is female biased. eSSD itself is probably an epiphenomenon of gendered evolutionary drivers whose strengths and directions are diverse. We demonstrate that eSSD spider clades are aberrant by sampling randomly across all spiders to establish overall averages for female (6.9 mm) and male (5.6 mm) size. At least 16 spider eSSD clades exist. We explore why the literature does not converge on an overall explanation for eSSD and propose an equilibrium model featuring clade- and context-specific drivers of gender size variation. eSSD affects other traits such as sexual cannibalism, genital damage, emasculation, and monogyny with terminal investment. Coevolution with these extreme sexual phenotypes is termed eSSD mating syndrome. Finally, as costs of female gigantism increase with size, eSSD may represent an evolutionary dead end.

Disturbances associated with agricultural intensification reduce our ability to achieve sustainable crop production. These disturbances stem from crop-management tactics and can leave crop fields more vulnerable to insect outbreaks, in part because natural-enemy communities often tend to be more susceptible to disturbance than herbivorous pests. Recent research has explored practices that conserve natural-enemy communities and reduce pest outbreaks, revealing that different components of agroecosystems can influence natural-enemy populations. In this review, we consider a range of disturbances that influence pest control provided by natural enemies and how conservation practices can mitigate or counteract disturbance. We use four case studies to illustrate how conservation and disturbance mitigation increase the potential for biological control and provide co-benefits for the broader agroecosystem. To facilitate the adoption of conservation practices that improve top-down control across significant areas of the landscape, these practices will need to provide multifunctional benefits, but should be implemented with natural enemies explicitly in mind.

The terrestrial arthropod fauna of wetlands has been largely ignored by scientists compared to other ecological elements, yet these organisms are among the most important influences on the ecology of these systems, with the vast majority of the biodiversity in wetlands found among the terrestrial arthropods. Wetlands present a range of habitat for terrestrial arthropods, with unique faunas being associated with soils and ground litter, living-plant substrates, and peatlands. Myriapoda, Araneae, Collembola, Carabidae, Formicidae, and assorted herbivorous Coleoptera and Lepidoptera are the terrestrial arthropod groups that most influence the ecology of wetlands. Despite their success, most terrestrial arthropods possess fairly rudimentary adaptations for life in wetlands, with most simply moving to higher ground or up vegetation during floods, although some species can tolerate immersion. Many terrestrial arthropods are environmentally sensitive and show considerable promise as bioindicators of wetland ecological conditions.

Although the insect circulatory system is involved in a multitude of vital physiological processes, it has gone grossly understudied. This review highlights this critical physiological system by detailing the structure and function of the circulatory organs, including the dorsal heart and the accessory pulsatile organs that supply hemolymph to the appendages. It also emphasizes how the circulatory system develops and ages and how, by means of reflex bleeding and functional integration with the immune system, it supports mechanisms for defense against predators and microbial invaders, respectively. Beyond that, this review details evolutionary trends and novelties associated with this system, as well as the ways in which this system also plays critical roles in thermoregulation and tracheal ventilation in high-performance fliers. Finally, this review highlights how novel discoveries could be harnessed for the control of vector-borne diseases and for translational medicine, and it details principal knowledge gaps that necessitate further investigation.

Symbiotic associations with microorganisms represent major sources of ecological and evolutionary innovations in insects. Multiple insect taxa engage in symbioses with bacteria of the genus Burkholderia, a diverse group that is widespread across different environments and whose members can be mutualistic or pathogenic to plants, fungi, and animals. Burkholderia symbionts provide nutritional benefits and resistance against insecticides to stinkbugs, defend Lagria beetle eggs against pathogenic fungi, and may be involved in nitrogen metabolism in ants. In contrast to many other insect symbioses, the known associations with Burkholderia are characterized by environmental symbiont acquisition or mixed-mode transmission, resulting in interesting ecological and evolutionary dynamics of symbiont strain composition. Insect–Burkholderia symbioses present valuable model systems from which to derive insights into general principles governing symbiotic interactions because they are often experimentally and genetically tractable and span a large fraction of the diversity of functions, localizations, and transmission routes represented in insect symbioses.

Parasitoids depend on other insects for the development of their offspring. Their eggs are laid in or on a host insect that is consumed during juvenile development. Parasitoids harbor a diversity of microbial symbionts including viruses, bacteria, and fungi. In contrast to symbionts of herbivorous and hematophagous insects, parasitoid symbionts do not provide nutrients. Instead, they are involved in parasitoid reproduction, suppression of host immune responses, and manipulation of the behavior of herbivorous hosts. Moreover, recent research has shown that parasitoid symbionts such as polydnaviruses may also influence plant-mediated interactions among members of plant-associated communities at different trophic levels, such as herbivores, parasitoids, and hyperparasitoids. This implies that these symbionts have a much more extended phenotype than previously thought. This review focuses on the effects of parasitoid symbionts on direct and indirect species interactions and the consequences for community ecology.

Dengue is an emerging viral disease principally transmitted by the Aedes (Stegomyia) aegypti mosquito. It is one of the fastest-growing global infectious diseases, with 100–400 million new infections a year, and is now entrenched in a growing number of tropical megacities. Behind this rapid rise is the simple adaptation of Ae. aegypti to a new entomological niche carved out by human habitation. This review describes the expansion of dengue and explores how key changes in the ecology of Ae. aegypti allowed it to become a successful invasive species and highly efficient disease vector. We argue that characterizing geographic heterogeneity in mosquito bionomics will be a key research priority that will enable us to better understand future dengue risk and design control strategies to reverse its global spread.

Bumble bees (Bombus) are unusually important pollinators, with approximately 260 wild species native to all biogeographic regions except sub-Saharan Africa, Australia, and New Zealand. As they are vitally important in natural ecosystems and to agricultural food production globally, the increase in reports of declining distribution and abundance over the past decade has led to an explosion of interest in bumble bee population decline. We summarize data on the threat status of wild bumble bee species across biogeographic regions, underscoring regions lacking assessment data. Focusing on data-rich studies, we also synthesize recent research on potential causes of population declines. There is evidence that habitat loss, changing climate, pathogen transmission, invasion of nonnative species, and pesticides, operating individually and in combination, negatively impact bumble bee health, and that effects may depend on species and locality. We distinguish between correlational and causal results, underscoring the importance of expanding experimental research beyond the study of two commercially available species to identify causal factors affecting the diversity of wild species.

Academic interest in plant natural products with insecticidal properties has continued to grow in the past 20 years, while commercialization of new botanical insecticides and market expansion of existing botanicals has lagged considerably behind. Insecticides based on pyrethrum and neem (azadirachtin) continue to be standard bearers in this class of pesticides, but globally, their increased presence is largely a consequence of introduction into new jurisdictions. Insecticides based on plant essential oils are just beginning to emerge as useful plant protectants. Some countries (such as Turkey, Uruguay, the United Arab Emirates, and Australia) have relaxed regulatory requirements for specific plant extracts and oils, while in North America and the European Union, stricter requirements have slowed progress toward commercialization of new products. Botanicals are likely to remain niche products in many agricultural regions and may have the greatest impact in developing countries in tropical regions where the source plants are readily available and conventional products are both expensive and dangerous to users.

Insects, like all eukaryotes, require sterols for structural and metabolic purposes. However, insects, like all arthropods, cannot make sterols. Cholesterol is the dominant tissue sterol for most insects; insect herbivores produce cholesterol by metabolizing phytosterols, but not always with high efficiency. Many insects grow on a mixed-sterol diet, but this ability varies depending on the types and ratio of dietary sterols. Dietary sterol uptake, transport, and metabolism are regulated by several proteins and processes that are relatively conserved across eukaryotes. Sterol requirements also impact insect ecology and behavior. There is potential to exploit insect sterol requirements to (a) control insect pests in agricultural systems and (b) better understand sterol biology, including in humans. We suggest that future studies focus on the genetic mechanism of sterol metabolism and reverse transportation, characterizing sterol distribution and function at the cellular level, the role of bacterial symbionts in sterol metabolism, and interrupting sterol trafficking for pest control.

With 20% of the world's population but just 7% of the arable land, China has invested heavily in crop biotechnology to increase agricultural productivity. We examine research on insect-resistant genetically engineered (IRGE) crops in China, including strategies to promote their sustainable use. IRGE cotton, rice, and corn lines have been developed and proven efficacious for controlling lepidopteran crop pests. Ecological impact studies have demonstrated conservation of natural enemies of crop pests and halo suppression of crop-pest populations on a local scale. Economic, social, and human health effects are largely positive and, in the case of Bt cotton, have proven sustainable over 20 years of commercial production. Wider adoption of IRGE crops in China is constrained by relatively limited innovation capacity, public misperception, and regulatory inaction, suggesting the need for further financial investment in innovation and greater scientific engagement with the public. The Chinese experience with Bt cotton might inform adoption of other Bt crops in China and other developing countries.

The RNA interference (RNAi) triggered by short/small interfering RNA (siRNA) was discovered in nematodes and found to function in most living organisms. RNAi has been widely used as a research tool to study gene functions and has shown great potential for the development of novel pest management strategies. RNAi is highly efficient and systemic in coleopterans but highly variable or inefficient in many other insects. Differences in double-stranded RNA (dsRNA) degradation, cellular uptake, inter- and intracellular transports, processing of dsRNA to siRNA, and RNA-induced silencing complex formation influence RNAi efficiency. The basic dsRNA delivery methods include microinjection, feeding, and soaking. To improve dsRNA delivery, various new technologies, including cationic liposome–assisted, nanoparticle-enabled, symbiont-mediated, and plant-mediated deliveries, have been developed. Major challenges to widespread use of RNAi in insect pest management include variable RNAi efficiency among insects, lack of reliable dsRNA delivery methods, off-target and nontarget effects, and potential development of resistance in insect populations.

Chikungunya virus (CHIKV), a re-emerging mosquito-borne arbovirus, has caused millions of cases of severe, often chronic arthralgia during recent outbreaks. In Africa, circulation in sylvatic, enzootic cycles involves several species of arboreal mosquito vectors that transmit among diverse nonhuman primates and possibly other amplifying hosts. Most disease occurs when CHIKV emerges into a human-amplified cycle involving Aedes aegypti and sometimes Aedes albopictus transmission and extensive spread via travelers. Epidemiologic studies suggest that the transition from enzootic to epidemic cycles begins when people are infected via spillover in forests. However, efficient human amplification likely only ensues far from enzootic habitats where peridomestic vector and human densities are adequate. Recent outbreaks have been enhanced by mutations that adapt CHIKV for more efficient infection of Ae. albopictus, allowing for geographic expansion. However, epistatic interactions, sometimes resulting from founder effects following point-source human introductions, have profound effects on transmission efficiency, making CHIKV emergence somewhat unpredictable.

Development of resistance in major grain insect pest species to the key fumigant phosphine (hydrogen phosphide) across the globe has put the viability and sustainability of phosphine in jeopardy. The resistance problem has been aggravated over the past two decades, due mostly to the lack of suitable alternatives matching the major attributes of phosphine, including its low price, ease of application, proven effectiveness against a broad pest spectrum, compatibility with most storage conditions, and international acceptance as a residue-free treatment. In this review, we critically analyze the published literature in the area of phosphine resistance with special emphasis on the methods available for detection of resistance, the genetic basis of resistance development, key management strategies, and research gaps that need to be addressed.

Tularemia is a Holarctic zoonosis caused by the gamma proteobacterium Francisella tularensis and is considered to be a vector-borne disease. In many regions, human risk is associated with the bites of flies, mosquitoes, or ticks. But the biology of the agent is such that risk may be fomite related, and large outbreaks can occur due to inhalation or ingestion of contaminated materials. Such well-documented human risk factors suggest a role for these risk factors in the enzootic cycle as well. Many arthropods support the growth or survival of the agent, but whether arthropods (ticks in particular) are obligately required for the perpetuation of F. tularensis remains to be demonstrated. As with most zoonoses, our knowledge of the ecology of F. tularensis has been driven with the objective of understanding human risk. In this review, we focus on the role of the arthropod in maintaining F. tularensis, particularly with respect to long-term enzootic persistence.

Whole-animal experiments devised to investigate possible association between photoperiodic time measurement and the circadian system (Bünning's hypothesis) are compared with more recent molecular investigations of circadian clock genes. In Sarcophaga argyrostoma and some other species, experimental cycles of light and darkness revealed a photoperiodic oscillator, set to constant phase at dusk and measuring night length repeatedly during extended periods of darkness. In some species, however, extreme dampening revealed an unrepetitive (i.e., hourglass-like) response. Rhythms of clock gene transcript abundance may also show similar phase relationships to the light cycle, and gene silencing of important clock genes indicates that they play a crucial role in photoperiodism either alone or in concert. However, the multiplicity of peripheral oscillators in the insect circadian system indicates that more complex mechanisms might also be important.