Annual Review of Entomology - Volume 63, 2018

This article presents an overview of the development of techniques for analyzing cuticular proteins (CPs), their transcripts, and their genes over the past 50 years based primarily on experience in the laboratory of J.H. Willis. It emphasizes changes in the kind of data that can be gathered and how such data provided insights into the molecular underpinnings of insect metamorphosis and cuticle structure. It describes the techniques that allowed visualization of the location of CPs at both the anatomical and intracuticular levels and measurement of the appearance and deployment of transcripts from CP genes as well as what was learned from genomic and transcriptomic data. Most of the early work was done with the cecropia silkmoth, Hyalophora cecropia, and later work was with Anopheles gambiae.

The ability to identify nutrient-rich food and avoid toxic substances is essential for an animal's survival. Although olfaction and vision contribute to food detection, the gustatory system acts as a final checkpoint control for food acceptance or rejection. The vinegar fly Drosophila melanogaster tastes many of the same stimuli as mammals and provides an excellent model system for comparative studies of taste detection. The relative simplicity of the fly brain and behaviors, along with the molecular genetic and functional approaches available in this system, allow the examination of gustatory neural circuits from sensory input to motor output. This review discusses the molecules and cells that detect taste compounds in the periphery and the circuits that process taste information in the brain. These studies are providing insight into how the detection of taste compounds regulates feeding decisions.

In the last decade, new methods of estimating global species richness have been developed and existing ones improved through the use of more appropriate statistical tools and new data. Taking the mean of most of these new estimates indicates that globally there are approximately 1.5 million, 5.5 million, and 7 million species of beetles, insects, and terrestrial arthropods, respectively. Previous estimates of 30 million species or more based on the host specificity of insects to plants now seem extremely unlikely. With 1 million insect species named, this suggests that 80% remain to be discovered and that a greater focus should be placed on less-studied taxa such as many families of Coleoptera, Diptera, and Hymenoptera and on poorly sampled parts of the world. DNA tools have revealed many new species in taxonomically intractable groups, but unbiased studies of previously well-researched insect faunas indicate that 1–2% of species may be truly cryptic.

Human commerce has resulted in the spread of the imported fire ants, Solenopsis species, worldwide. Six species of parasitic Pseudacteon phorid flies that are highly host specific to the Solenopsis saevissima complex of Solenopsis fire ants have been successfully released in the southern United States. The presence of Pseudacteon phorid flies, in addition to having direct mortality effects on their host ants, modifies foraging behavior and disrupts interspecific competition between host species and other ant species in the community. Fire ant workers have evolved effective methods to cope with parasitism pressure, which may relieve population-level impacts of introduced phorid flies. This review focuses on the mechanisms underlying host location, host preference, and host-size selection of Pseudacteon phorid flies and highlights their direct and indirect effects on fire ant populations. Knowledge gained from parasitoid–ant interactions will enhance use of natural enemies as biological control agents for invasive social insects.

Sleep is essential for proper brain function in mammals and insects. During sleep, animals are disconnected from the external world; they show high arousal thresholds and changed brain activity. Sleep deprivation results in a sleep rebound. Research using the fruit fly, Drosophila melanogaster, has helped us understand the genetic and neuronal control of sleep. Genes involved in sleep control code for ion channels, factors influencing neurotransmission and neuromodulation, and proteins involved in the circadian clock. The neurotransmitters/neuromodulators involved in sleep control are GABA, dopamine, acetylcholine, serotonin, and several neuropeptides. Sleep is controlled by the interplay between sleep homeostasis and the circadian clock. Putative sleep-wake centers are located in higher-order brain centers that are indirectly connected to the circadian clock network. The primary function of sleep appears to be the downscaling of synapses that have been built up during wakefulness. Thus, brain homeostasis is maintained and learning and memory are assured.

The discovery of an odd virus from hematophagous arthropods 40 years ago by Stollar and Thomas described cell fusing agent virus in cells derived from Aedes aegypti mosquitoes. Then came the report of Kamiti River virus from Ae. macintoshi in 1999, followed by worldwide reports of the discovery of other viruses of mosquitoes, ticks, and midges that replicate only in arthropods and not in vertebrates or in vertebrate cells. These viruses (now totaling at least 64 published) have genomes analogous to viruses in various families that include arboviruses and nonarboviruses. It is likely that some of these viruses have been insufficiently studied and may yet be shown to infect vertebrates. However, there is no doubt that the vast majority are restricted to arthropods alone and that they represent a recently recognized clade. Their biology, modes of transmission, worldwide distribution (some have been detected in wild-caught mosquitoes in both Asia and the United States, for example), molecular characteristics of their genomes, and potential for becoming vertebrate pathogens, or at least serving as virus reservoirs, are fascinating and may provide evidence useful in understanding virus evolution. Because metagenomics studies of arthropods have shown that arthropod genomes are the sources of arthropod virus genomes, further studies may also provide insights into the evolution of arthropods. More recently, others have published excellent papers that briefly review discoveries of arthropod viruses and that characterize certain genomic peculiarities, but, to now, there have been no reviews that encompass all these facets. We therefore anticipate that this review is published at a time and in a manner that is helpful for both virologists and entomologists to make more sense and understanding of this recently recognized and obviously important virus group. This review focuses specifically on arthropod viruses in hematophagous arthropods.

Social insect colonies have evolved many collectively performed adaptations that reduce the impact of infectious disease and that are expected to maximize their fitness. This colony-level protection is termed social immunity, and it enhances the health and survival of the colony. In this review, we address how social immunity emerges from its mechanistic components to produce colony-level disease avoidance, resistance, and tolerance. To understand the evolutionary causes and consequences of social immunity, we highlight the need for studies that evaluate the effects of social immunity on colony fitness. We discuss the roles that host life history and ecology have on predicted eco-evolutionary dynamics, which differ among the social insect lineages. Throughout the review, we highlight current gaps in our knowledge and promising avenues for future research, which we hope will bring us closer to an integrated understanding of socio-eco-evo-immunology.

Neonicotinoids (neonics) are remarkably effective as plant systemics to control sucking insects and for flea control on dogs and cats. The nitroimines imidacloprid, clothianidin, thiamethoxam, and dinotefuran are the leaders among the seven commercial neonics that also include the nitromethylene nitenpyram, the nitromethylene-derived cycloxaprid, and the cyanoimines acetamiprid and thiacloprid. Honey bees are highly sensitive to the nitroimines and nitromethylenes, but the cyanoimines are less toxic. All neonics are nicotinic acetylcholine receptor (nAChR) agonists with a common mode of action, target-site cross-resistance, and much higher potency on insect than mammalian nAChRs at defined binding sites. The structurally related sulfoximine sulfoxaflor and butenolide flupyradifurone are also nAChR agonists, and the mesoionic triflumezopyrim is a nAChR competitive modulator with little or no target-site cross-resistance. Some neonics induce stress tolerance in plants via salicylate-associated systems. The neonics in general are readily metabolized and, except for pollinators, have favorable toxicological profiles.

As holometabolous insects that occupy distinct aquatic and terrestrial environments in larval and adult stages and utilize hematophagy for nutrient acquisition, mosquitoes are subjected to a wide variety of symbiotic interactions. Indeed, mosquitoes play host to endosymbiotic, entomopathogenic, and mosquito-borne organisms, including protozoa, viruses, bacteria, fungi, fungal-like organisms, and metazoans, all of which trigger and shape innate infection-response capacity. Depending on the infection or interaction, the mosquito may employ, for example, cellular and humoral immune effectors for septic infections in the hemocoel, humoral infection responses in the midgut lumen, and RNA interference and programmed cell death for intracellular pathogens. These responses often function in concert, regardless of the infection type, and provide a robust front to combat infection. Mosquito-borne pathogens and entomopathogens overcome these immune responses, employing avoidance or suppression strategies. Burgeoning methodologies are capitalizing on this concerted deployment of immune responses to control mosquito-borne disease.

The transmission of insect-borne plant pathogens, including viruses, bacteria, phytoplasmas, and fungi depends upon the abundance and behavior of their vectors. These pathogens should therefore be selected to influence their vectors to enhance their transmission, either indirectly, through the infected host plant, or directly, after acquisition of the pathogen by the vector. Accumulating evidence provides partial support for the occurrence of vector manipulation by plant pathogens, especially for plant viruses, for which a theoretical framework can explain patterns in the specific effects on vector behavior and performance depending on their modes of transmission. The variability in effects of pathogens on their vectors, however, suggests inconsistency in the occurrence of vector manipulation but also may reflect incomplete information about these systems. For example, manipulation can occur through combinations of specific effects, including direct and indirect effects on performance and behavior, and dynamics in those effects with disease progression or pathogen acquisition that together constitute syndromes that promote pathogen spread. Deciphering the prevalence and forms of vector manipulation by plant pathogens remains a compelling field of inquiry, but gaps and opportunities to advance it remain. A proposed research agenda includes examining vector manipulation syndromes comprehensively within pathosystems, expanding the taxonomic and genetic breadth of the systems studied, evaluating dynamic effects that occur during disease progression, incorporating the influence of biotic and abiotic environmental factors, evaluating the effectiveness of putative manipulation syndromes under field conditions, deciphering chemical and molecular mechanisms whereby pathogens can influence vectors, expanding the use of evolutionary and epidemiological models, and seeking opportunities to exploit these effects to improve management of insect-borne, economically important plant pathogens. We expect this field to remain vibrant and productive in its own right and as part of a wider inquiry concerning host and vector manipulation by plant and animal pathogens and parasites.

Viticulture has experienced dramatic global growth in acreage and value. As the international exchange of goods has increased, so too has the market demand for sustainably produced products. Both elements redefine the entomological challenges posed to viticulture and have stimulated significant advances in arthropod pest control programs. Vineyard managers on all continents are increasingly combating invasive species, resulting in the adoption of novel insecticides, semiochemicals, and molecular tools to support sustainable viticulture. At the local level, vineyard management practices consider factors such as the surrounding natural ecosystem, risk to fish populations, and air quality. Coordinated multinational responses to pest invasion have been highly effective and have, for example, resulted in eradication of the moth Lobesia botrana from California vineyards, a pest found in 2009 and eradicated by 2016. At the global level, the shared pests and solutions for their suppression will play an increasing role in delivering internationally sensitive pest management programs that respond to invasive pests, climate change, novel vector and pathogen relationships, and pesticide restrictions.

The Australian cotton industry progressively embraced integrated pest management (IPM) to alleviate escalating insecticide resistance issues. A systems IPM approach was used with core principles that were built around pest ecology/biology and insecticide resistance management; together, these were integrated into a flexible, year-round approach that facilitated easy incorporation of new science, strategies, and pests. The approach emphasized both strategic and tactical elements to reduce pest abundance and rationalize decisions about pest control, with insecticides as a last resort. Industry involvement in developing the approach was vital to embedding IPM within the farming system. Adoption of IPM was facilitated by the introduction of Bt cotton, availability of selective insecticides, economic validation, and an industry-wide extension campaign. Surveys indicate IPM is now embedded in industry, confirming the effectiveness of an industry-led, backed-by-science approach. The amount of insecticide active ingredient applied per hectare against pests has also declined dramatically. Though challenges remain, pest management has transitioned from reactively attempting to eradicate pests from fields to proactively managing them year-round, considering the farm within the wider landscape.

The South American tomato pinworm, Tuta absoluta (Meyrick), is native to the western Neotropics. After invading Spain in 2006, it spread rapidly throughout Afro-Eurasia and has become a major threat to world tomato production. Integrated pest management (IPM) strategies have been developed, but widespread insecticide use has caused selection for insecticide resistance as well as undesirable effects on key beneficial arthropods. Augmentation and conservation biological control relying on omnivorous mirid predators has proved successful for management of T. absoluta, where implementation is dependent on abiotic, biotic (e.g., alternative prey), and anthropogenic factors (e.g., pesticides). Research has been carried out on larval parasitoids, showing potential for further development of sustainable control. The development of resistant tomato varieties is ongoing, but they are not commercially available yet. Knowledge gaps remain to be filled to optimize IPM packages on tomato crops and to help prevent further spread worldwide.

Under the superorganism concept, insect societies are so tightly integrated that they possess features analogous to those of single organisms, including collective cognition. If so, colony function might fruitfully be studied using methods developed to understand individual animals. Here, we review research that uses psychological approaches to understand decision making by colonies. The application of neural models to collective choice shows fundamental similarities between how brains and colonies balance speed/accuracy trade-offs in decision making. Experimental analyses have explored collective rationality, cognitive capacity, and perceptual discrimination at both individual and colony levels. A major theme is the emergence of improved colony-level function from interactions among relatively less capable individuals. However, colonies also encounter performance costs due to their reliance on positive feedback, which generates consensus but can also amplify errors. Collective learning is a nascent field for the further application of psychological methods to colonies. The research strategy reviewed here shows how the superorganism concept can serve as more than an illustrative analogy.

Monarch butterflies (Danaus plexippus) are familiar herbivores of milkweeds of the genus Asclepias, and most monarchs migrate each year to locate these host plants across North American ecosystems now dominated by agriculture. Eastern migrants overwinter in high-elevation forests in Mexico, and western monarchs overwinter in trees on the coast of California. Both populations face three primary threats to their viability: (a) loss of milkweed resources for larvae due to genetically modified crops, pesticides, and fertilizers; (b) loss of nectar resources from flowering plants; and (c) degraded overwintering forest habitats due to commercially motivated deforestation and other economic activities. Secondary threats to population viability include (d) climate change effects on milkweed host plants and the dynamics of breeding, overwintering, and migration; (e) the influence of invasive plants and natural enemies; (f) habitat fragmentation and coalescence that promote homogeneous, species-depleted landscapes; and (g) deliberate culture and release of monarchs and invasive milkweeds.

Insects can experience functional hypoxia, a situation in which O2 supply is inadequate to meet oxygen demand. Assessing when functional hypoxia occurs is complex, because responses are graded, age and tissue dependent, and compensatory. Here, we compare information gained from metabolomics and transcriptional approaches and by manipulation of the partial pressure of oxygen. Functional hypoxia produces graded damage, including damaged macromolecules and inflammation. Insects respond by compensatory physiological and morphological changes in the tracheal system, metabolic reorganization, and suppression of activity, feeding, and growth. There is evidence for functional hypoxia in eggs, near the end of juvenile instars, and during molting. Functional hypoxia is more likely in species with lower O2 availability or transport capacities and when O2 need is great. Functional hypoxia occurs normally during insect development and is a factor in mediating life-history trade-offs.

Honey bees feed on floral nectar and pollen that they store in their colonies as honey and bee bread. Social division of labor enables the collection of stores of food that are consumed by within-hive bees that convert stored pollen and honey into royal jelly. Royal jelly and other glandular secretions are the primary food of growing larvae and of the queen but are also fed to other colony members. Research clearly shows that bees regulate their intake, like other animals, around specific proportions of macronutrients. This form of regulation is done as individuals and at the colony level by foragers.

Insect invasions, the establishment and spread of nonnative insects in new regions, can have extensive economic and environmental consequences. Increased global connectivity accelerates rates of introductions, while climate change may decrease the barriers to invader species’ spread. We follow an individual-level insect- and arachnid-centered perspective to assess how the process of invasion is influenced by phenotypic heterogeneity associated with dispersal and stress resistance, and their coupling, across the multiple steps of the invasion process. We also provide an overview and synthesis on the importance of environmental filters during the entire invasion process for the facilitation or inhibition of invasive insect population spread. Finally, we highlight important research gaps and the relevance and applicability of ongoing natural range expansions in the context of climate change to gain essential mechanistic insights into insect invasions.

The muscid genus Philornis comprises approximately 50 described species of flies, nearly all of which are obligate parasites of nestling birds. Philornis species are native to the Neotropics and widely distributed from Florida to Argentina. Most research on this group has focused on P. downsi, which was introduced to the Galápagos Islands in the late twentieth century. Although Philornis parasitism kills nestlings in several native host species, nowhere do the effects seem more severe than in P. downsi in the Galápagos. Here, we review studies of native and introduced Philornis in an attempt to identify factors that may influence virulence and consider implications for the conservation of hosts in the Galápagos.