Annual Review of Entomology - Volume 60, 2015

In this highly personal account of my career in science, I try to show how many others influenced its course. I was able to abandon work in pure chemistry and microbiology and to take up research in entomology only with the help of others. My faith in the value of collaborative, interdisciplinary work has been the key to success. Our focus on proteins of insect hemolymph has provided valuable insights into insect biochemistry and physiology.

All insects are colonized by microorganisms on the insect exoskeleton, in the gut and hemocoel, and within insect cells. The insect microbiota is generally different from microorganisms in the external environment, including ingested food. Specifically, certain microbial taxa are favored by the conditions and resources in the insect habitat, by their tolerance of insect immunity, and by specific mechanisms for their transmission. The resident microorganisms can promote insect fitness by contributing to nutrition, especially by providing essential amino acids, B vitamins, and, for fungal partners, sterols. Some microorganisms protect their insect hosts against pathogens, parasitoids, and other parasites by synthesizing specific toxins or modifying the insect immune system. Priorities for future research include elucidation of microbial contributions to detoxification, especially of plant allelochemicals in phytophagous insects, and resistance to pathogens; as well as their role in among-insect communication; and the potential value of manipulation of the microbiota to control insect pests.

Crop domestication is the process of artificially selecting plants to increase their suitability to human requirements: taste, yield, storage, and cultivation practices. There is increasing evidence that crop domestication can profoundly alter interactions among plants, herbivores, and their natural enemies. Overall, little is known about how these interactions are affected by domestication in the geographical ranges where these crops originate, where they are sympatric with the ancestral plant and share the associated arthropod community. In general, domestication consistently has reduced chemical resistance against herbivorous insects, improving herbivore and natural enemy performance on crop plants. More studies are needed to understand how changes in morphology and resistance-related traits arising from domestication may interact with environmental variation to affect species interactions across multiple scales in agroecosystems and natural ecosystems.

Insect heat shock proteins include ATP-independent small heat shock proteins and the larger ATP-dependent proteins, Hsp70, Hsp90, and Hsp60. In concert with cochaperones and accessory proteins, heat shock proteins mediate essential activities such as protein folding, localization, and degradation. Heat shock proteins are synthesized constitutively in insects and induced by stressors such as heat, cold, crowding, and anoxia. Synthesis depends on the physiological state of the insect, but the common function of heat shock proteins, often working in networks, is to maintain cell homeostasis through interaction with substrate proteins. Stress-induced expression of heat shock protein genes occurs in a background of protein synthesis inhibition, but in the course of diapause, a state of dormancy and increased stress tolerance, these genes undergo differential regulation without the general disruption of protein production. During diapause, when ATP concentrations are low, heat shock proteins may sequester rather than fold proteins.

Termites have many unique evolutionary adaptations associated with their eusocial lifestyles. Recent omics research has created a wealth of new information in numerous areas of termite biology (e.g., caste polyphenism, lignocellulose digestion, and microbial symbiosis) with wide-ranging applications in diverse biotechnological niches. Termite biotechnology falls into two categories: (a) termite-targeted biotechnology for pest management purposes, and (b) termite-modeled biotechnology for use in various industrial applications. The first category includes several candidate termiticidal modes of action such as RNA interference, digestive inhibition, pathogen enhancement, antimicrobials, endocrine disruption, and primer pheromone mimicry. In the second category, termite digestomes are deep resources for host and symbiont lignocellulases and other enzymes with applications in a variety of biomass, industrial, and processing applications. Moving forward, one of the most important approaches for accelerating advances in both termite-targeted and termite-modeled biotechnology will be to consider host and symbiont together as a single functional unit.

Miniaturization leads to considerable reorganization of structures in insects, affecting almost all organs and tissues. In the smallest insects, comparable in size to unicellular organisms, modifications arise not only at the level of organs, but also at the cellular level. Miniaturization is accompanied by allometric changes in many organ systems. The consequences of miniaturization displayed by different insect taxa include both common and unique changes. Because the smallest insects are among the smallest metazoans and have the most complex organization among organisms of the same size, their peculiar structural features and the factors that limit their miniaturization are of considerable theoretical interest to general biology.

All climate change scenarios predict an increase in both global temperature means and the magnitude of seasonal and diel temperature variation. The nonlinear relationship between temperature and biological processes means that fluctuating temperatures lead to physiological, life history, and ecological consequences for ectothermic insects that diverge from those predicted from constant temperatures. Fluctuating temperatures that remain within permissive temperature ranges generally improve performance. By contrast, those which extend to stressful temperatures may have either positive impacts, allowing repair of damage accrued during exposure to thermal extremes, or negative impacts from cumulative damage during successive exposures. We discuss the mechanisms underlying these differing effects. Fluctuating temperatures could be used to enhance or weaken insects in applied rearing programs, and any prediction of insect performance in the field—including models of climate change or population performance—must account for the effect of fluctuating temperatures.

The developmental mechanisms that control body size and the relative sizes of body parts are today best understood in insects. Size is controlled by the mechanisms that cause growth to stop when a size characteristic of the species has been achieved. This requires the mechanisms to assess size and respond by stopping the process that controls growth. Growth is controlled by two hormones, insulin and ecdysone, that act synergistically by controlling cell growth and cell division. Ecdysone has two distinct functions: At low concentration it controls growth, and at high levels it causes molting and tissue differentiation. Growth is stopped by the pulse of ecdysone that initiates the metamorphic molt. Body size is sensed by either stretch receptors or oxygen restriction, depending on the species, which stimulate the high level of ecdysone secretion that induces a molt. Wing growth occurs mostly after the body has stopped growing. Wing size is adjusted to body size by variation in both the duration and level of ecdysone secretion.

Opiliones are one of the largest arachnid orders, with more than 6,500 species in 50 families. Many of these families have been erected or reorganized in the last few years since the publication of The Biology of Opiliones. Recent years have also seen an explosion in phylogenetic work on Opiliones, as well as in studies using Opiliones as test cases to address biogeographic and evolutionary questions more broadly. Accelerated activity in the study of Opiliones evolution has been facilitated by the discovery of several key fossils, including the oldest known Opiliones fossil, which represents a new, extinct suborder. Study of the group's biology has also benefited from rapid accrual of genomic resources, particularly with respect to transcriptomes and functional genetic tools. The rapid emergence and utility of Phalangium opilio as a model for evolutionary developmental biology of arthropods serve as demonstrative evidence of a new area of study in Opiliones biology, made possible through transcriptomic data.

Differential regulation at the level of transcription provides a means for controlling gene expression in eukaryotes, especially during development. Insect model systems have been extensively used to decipher the molecular basis of such regulatory cascades, and one of the oldest such model systems is the regulation of chorion gene expression during ovarian follicle maturation. Recent experimental and technological advances have shed new light onto the system, allowing us to revisit it. Thus, in this review we try to summarize almost 40 years' worth of studies on chorion gene regulation while—by comparing Bombyx mori and Drosophila melanogaster models—attempting to present a comprehensive, unified model of the various regulatory aspects of choriogenesis that takes into account the evolutionary conservation and divergence of the underlying mechanisms.

Parasitoids of the hymenopterous family Encyrtidae are one of the most important groups of natural enemies of soft scale insects and have been used extensively in biological control. We summarize existing knowledge of the biology, ecology, and behavior of these parasitoids and how it relates to biological control. Soft scale stage/size and phenology are important determinants of host range and host utilization, which are key aspects in understanding how control by these parasitoids is exerted. Furthermore, the nutritional ecology of encyrtids and their physiological interactions with their hosts affect soft scale insect population dynamics. Lastly, the interactions among encyrtids, heteronomous parasitoids, and ants shape parasitoid species complexes and consequently have a direct impact on the biological control of soft scale insects.

Plants secrete extrafloral nectar (EFN) as an induced defense against herbivores. EFN contains not only carbohydrates and amino acids but also pathogenesis-related proteins and other protective enzymes, making EFN an exclusive reward. EFN secretion is commonly induced after wounding, likely owing to a jasmonic acid–induced cell wall invertase, and is limited by phloem sucrose availability: Both factors control EFN secretion according to the optimal defense hypothesis. Non-ant EFN consumers include parasitoids, wasps, spiders, mites, bugs, and predatory beetles. Little is known about the relevance of EFN to the nutrition of its consumers and, hence, to the structuring of arthropod communities. The mutualism can be established quickly among noncoevolved (e.g., invasive) species, indicating its easy assembly is due to ecological fitting. Therefore, increasing efforts are directed toward using EFN in biocontrol. However, documentation of the importance of EFN for the communities of plants and arthropods in natural, invasive, and agricultural ecosystems is still limited.

Plant protease inhibitors (PIs) are natural plant defense proteins that inhibit proteases of invading insect herbivores. However, their anti-insect efficacy is determined not only by their potency toward a vulnerable insect system but also by the response of the insect to such a challenge. Through the long history of coevolution with their host plants, insects have developed sophisticated mechanisms to circumvent antinutritional effects of dietary challenges. Their response takes the form of changes in gene expression and the protein repertoire in cells lining the alimentary tract, the first line of defense. Research in insect digestive proteases has revealed the crucial roles they play in insect adaptation to plant PIs and has brought about a new appreciation of how phytophagous insects employ this group of molecules in both protein digestion and counterdefense. This review provides researchers in related fields an up-to-date summary of recent advances.

This article reviews the latest developments in our understanding of the origin, development, and evolution of nymphalid butterfly eyespots. Recent contributions to this field include insights into the evolutionary and developmental origin of eyespots and their ancestral deployment on the wing, the evolution of eyespot number and eyespot sexual dimorphism, and the identification of genes affecting eyespot development and black pigmentation. I also compare features of old and more recently proposed models of eyespot development and propose a schematic for the genetic regulatory architecture of eyespots. Using this schematic I propose two hypotheses for why we observe limits to morphological diversity across these serially homologous traits.

Whiteflies are small hemipterans numbering more than 1,550 described species, of which about 50 are agricultural pests. Adults are free-living, whereas late first to fourth instars are sessile on the plant. All known species of whitefly parasitoids belong to Hymenoptera; two genera, Encarsia and Eretmocerus, occur worldwide, and others are mostly specific to different continents. All parasitoid eggs are laid in—or in Eretmocerus, under—the host. They develop within whitefly nymphs and emerge from the fourth instar, and in Cales, from either the third or fourth instar. Parasitized hosts are recognized by conspecifics, but super- and hyperparasitism occur. Dispersal flights are influenced by gender and mating status, but no long-range attraction to whitefly presence on leaves is known. Studies on En. formosa have laid the foundation for behavioral studies and biological control in general. We review past and ongoing studies of whitefly parasitoids worldwide, updating available information on species diversity, biology, behavior, tritrophic interactions, and utilization in pest management.

In this review we highlight recent advances in four areas in which nutrition shapes the relationships between organisms: between plants and herbivores, between hosts and their microbiota, between individuals within groups and societies, and between species within food webs. We demonstrate that taking an explicitly multidimensional view of nutrition and employing the logic of the geometric framework for nutrition provide novel insights and offer a means of integration across different levels of organization, from individuals to ecosystems.

Wireworms, the larvae of click beetles (Coleoptera: Elateridae), have had a centuries-long role as major soil insect pests worldwide. With insecticidal control options dwindling, research on click beetle biology and ecology is of increasing importance in the development of new control tactics. Methodological improvements have deepened our understanding of how larvae and adults spatially and temporarily utilize agricultural habitats and interact with their environment. This progress, however, rests with a few pest species, and efforts to obtain comparable knowledge on other economically important elaterids are crucial. There are still considerable gaps in our understanding of female and larval ecology; movement of elaterids within landscapes; and the impact of natural enemies, cultivation practices, and environmental change on elaterid population dynamics. This knowledge will allow generation of multifaceted control strategies, including cultural, physical, and chemical measures, tailored toward species complexes and crops across a range of appropriate spatial scales.

The major malaria vectors of the Southwest Pacific belong to a group of closely related mosquitoes known as the Anopheles punctulatus group. The group comprises 13 co-occurring species that either are isomorphic or carry overlapping morphological features, and today several species remain informally named. The advent of species-diagnostic molecular tools in the 1990s permitted a new raft of studies into the newly differentiated mosquitoes of this group, and these have revealed five species as the region's primary malaria vectors: An. farauti, An. hinesorum, An. farauti 4, An. koliensis, and An. punctulatus. Species' distributions are now well established across Papua New Guinea, northern Australia, and the Solomon Archipelago, but little has been documented thus far in eastern Indonesia. As each species reveals significant differences in distribution and biology, the relative paucity of knowledge of their biology or ecology in relation to malaria transmission is brought into clearer focus. Only three of the species have undergone some form of spatial or population genetics analyses, and this has revealed striking differences in their genetic signatures throughout the region. This review compiles and dissects the key findings for this important mosquito group and points to where future research should focus to maximize the output of field studies in developing relevant knowledge on these malaria vectors.

Tsetse flies (Glossina spp.), vectors of African trypanosomes, are distinguished by their specialized reproductive biology, defined by adenotrophic viviparity (maternal nourishment of progeny by glandular secretions followed by live birth). This trait has evolved infrequently among insects and requires unique reproductive mechanisms. A key event in Glossina reproduction involves the transition between periods of lactation and nonlactation (dry periods). Increased lipolysis, nutrient transfer to the milk gland, and milk-specific protein production characterize lactation, which terminates at the birth of the progeny and is followed by a period of involution. The dry stage coincides with embryogenesis of the progeny, during which lipid reserves accumulate in preparation for the next round of lactation. The obligate bacterial symbiont Wigglesworthia glossinidia is critical to tsetse reproduction and likely provides B vitamins required for metabolic processes underlying lactation and/or progeny development. Here we describe findings that utilized transcriptomics, physiological assays, and RNA interference–based functional analysis to understand different components of adenotrophic viviparity in tsetse flies.