Annual Review of Entomology - Volume 61, 2016

This comprehensive review of the structure of sperm in all orders of insects evaluates phylogenetic implications, with the background of a phylogeny based on transcriptomes. Sperm characters strongly support several major branches of the phylogeny of insects—for instance, Cercophora, Dicondylia, and Psocodea—and also different infraordinal groups. Some closely related taxa, such as Trichoptera and Lepidoptera (Amphiesmenoptera), differ greatly in sperm structure. Sperm characters are very conservative in some groups (Heteroptera, Odonata) but highly variable in others, including Zoraptera, a small and morphologically uniform group with a tremendously accelerated rate of sperm evolution. Unusual patterns such as sperm dimorphism, the formation of bundles, or aflagellate and immotile sperm have evolved independently in several groups.

Studies of the migration of the eastern North American monarch butterfly (Danaus plexippus) have revealed mechanisms behind its navigation. The main orientation mechanism uses a time-compensated sun compass during both the migration south and the remigration north. Daylight cues, such as the sun itself and polarized light, are processed through both eyes and integrated through intricate circuitry in the brain's central complex, the presumed site of the sun compass. Monarch circadian clocks have a distinct molecular mechanism, and those that reside in the antennae provide time compensation. Recent evidence shows that migrants can also use a light-dependent inclination magnetic compass for orientation in the absence of directional daylight cues. The monarch genome has been sequenced, and genetic strategies using nuclease-based technologies have been developed to edit specific genes. The monarch butterfly has emerged as a model system to study the neural, molecular, and genetic basis of long-distance animal migration.

More than six decades after the onset of wide-scale commercial use of synthetic pesticides and more than fifty years after Rachel Carson's Silent Spring, pesticides, particularly insecticides, arguably remain the most influential pest management tool around the globe. Nevertheless, pesticide use is still a controversial issue and is at the regulatory forefront in most countries. The older generation of insecticide groups has been largely replaced by a plethora of novel molecules that exhibit improved human and environmental safety profiles. However, the use of such compounds is guided by their short-term efficacy; the indirect and subtler effects on their target species, namely arthropod pest species, have been neglected. Curiously, comprehensive risk assessments have increasingly explored effects on nontarget species, contrasting with the majority of efforts focused on the target arthropod pest species. The present review mitigates this shortcoming by hierarchically exploring within an ecotoxicology framework applied to integrated pest management the myriad effects of insecticide use on arthropod pest species.

Animals moving through the world are surrounded by potential information. But the components of this rich array that they extract will depend on current behavioral requirements and the animal's own sensory apparatus. Here, we consider the types of information available to social hymenopteran insects, with a specific focus on ants. This topic has a long history and much is known about how ants and other insects use idiothetic information, sky compasses, visual cues, and odor trails. Recent research has highlighted how insects use other sensory information for navigation, such as the olfactory cues provided by the environment. These cues are harder to understand because they submit less easily to anthropomorphic analysis. Here, we take an ecological approach, considering first what information is available to insects, then how different cues might interact, and finally we discuss potential neural correlates of these behaviors.

China is the world's fourth-largest country in terms of landmass. Its highly diverse biogeography presents opportunities for many invasive alien insects. However, physical and climate barriers sometimes prevent locally occurring species from spreading. China has 560 confirmed invasive alien species; 125 are insect pests, and 92 of these damage the agricultural ecosystem. The estimated annual economic loss due to alien invasive species is more than $18.9 billion. The most harmful invasive insects exhibit some common characteristics, such as high reproduction, competitive dominance, and high tolerance, and benefit from mutualist facilitation interactions. Regional cropping system structure adjustments have resulted in mono-agricultural ecosystems in cotton and other staple crops, providing opportunities for monophagous insect pests. Furthermore, human dietary shifts to fruits and vegetables and smallholder-based farming systems result in highly diverse agricultural ecosystems, which provide resource opportunities for polyphagous insects. Multiple cropping and widespread use of greenhouses provide continuous food and winter habitats for insect pests, greatly extending their geographic range. The current management system consists of early-warning, monitoring, eradication, and spread blocking technologies. This review provides valuable new synthetic information on integrated management practices based mainly on biological control for a number of invasive species. We encourage farmers and extension workers to be more involved in training and further research for novel protection methods that takes into consideration end users' needs.

Moth sexual pheromones are widely studied as a fine-tuned system of intraspecific sexual communication that reinforces interspecific reproductive isolation. However, their evolution poses a dilemma: How can the female pheromone and male preference simultaneously change to create a new pattern of species-specific attraction? Solving this puzzle requires us to identify the genes underlying intraspecific variation in signals and responses and to understand the evolutionary mechanisms responsible for their interspecific divergence. Candidate gene approaches and functional analyses have yielded insights into large families of biosynthetic enzymes and pheromone receptors, although the factors controlling their expression remain largely unexplored. Intra- and interspecific crosses have provided tantalizing evidence of regulatory genes, although, to date, mapping resolution has been insufficient to identify them. Recent advances in high-throughput genome and transcriptome sequencing, together with established techniques, have great potential to help scientists identify the specific genetic changes underlying divergence and resolve the mystery of how moth sexual communication systems evolve.

The Antarctic region comprises the continent, the Maritime Antarctic, the sub-Antarctic islands, and the southern cold temperate islands. Continental Antarctica is devoid of insects, but elsewhere diversity varies from 2 to more than 200 species, of which flies and beetles constitute the majority. Much is known about the drivers of this diversity at local and regional scales; current climate and glacial history play important roles. Investigations of responses to low temperatures, dry conditions, and varying salinity have spanned the ecological to the genomic, revealing new insights into how insects respond to stressful conditions. Biological invasions are common across much of the region and are expected to increase as climates become warmer. The drivers of invasion are reasonably well understood, although less is known about the impacts of invasion. Antarctic entomology has advanced considerably over the past 50 years, but key areas, such as interspecific interactions, remain underexplored.

Remote sensing describes the characterization of the status of objects and/or the classification of their identity based on a combination of spectral features extracted from reflectance or transmission profiles of radiometric energy. Remote sensing can be benchtop based, and therefore acquired at a high spatial resolution, or airborne at lower spatial resolution to cover large areas. Despite important challenges, airborne remote sensing technologies will undoubtedly be of major importance in optimized management of agricultural systems in the twenty-first century. Benchtop remote sensing applications are becoming important in insect systematics and in phenomics studies of insect behavior and physiology. This review highlights how remote sensing influences entomological research by enabling scientists to nondestructively monitor how individual insects respond to treatments and ambient conditions. Furthermore, novel remote sensing technologies are creating intriguing interdisciplinary bridges between entomology and disciplines such as informatics and electrical engineering.

Traumatic myiasis, the parasitic infestation by fly larvae in traumatic lesions of the tissues of living vertebrates, is a serious medical condition in humans and a welfare and economic issue in domestic animals. New molecular studies are providing insights into its evolution and epidemiology. Nevertheless, its incidence in humans is generally underreported, particularly in tropical and subtropical regions. Myiasis in domestic animals has been studied more extensively, but continuous management is difficult and expensive. A key concern is the inadvertent introduction and global spread of agents of myiasis into nonendemic areas, facilitated by climate change and global transport. The incursion of the New World screwworm fly (Cochliomyia hominivorax) into Libya is the most notable of many such range shifts and demonstrates the potential risks of these parasites and the costs of removing them once established in a geographic area. Nevertheless, the insect agents of myiasis can be of societal benefit to forensic science and in medicine as an aid to wound treatment (larval therapy).

Chitin is a major component of the exoskeleton and the peritrophic matrix of insects. It forms complex structures in association with different assortments of cuticle and peritrophic matrix proteins to yield biocomposites with a wide range of physicochemical and mechanical properties. The growth and development of insects are intimately coupled with the biosynthesis, turnover, and modification of chitin. The genes encoding numerous enzymes of chitin metabolism and proteins that associate with and organize chitin have been uncovered by bioinformatics analyses. Many of these proteins are encoded by sets of large gene families. There is specialization among members within each family, which function in particular tissues or developmental stages. Chitin-containing matrices are dynamically modified at every developmental stage and are under developmental and/or physiological control. A thorough understanding of the diverse processes associated with the assembly and turnover of these chitinous matrices offers many strategies to achieve selective pest control.

With 6,000 species, Neuroptera (lacewings, antlions, dustywings, and allies) is a relatively small order; however, most larval neuropterans are predacious, often in agricultural systems, lending added importance to this group. Advances in neuropteran phylogeny, most recently through genomic studies, stabilized the nomenclature of this ancestral order of Holometabola, facilitating basic and applied research on these important and interesting insects. The first pheromones for green lacewings (Chrysopidae) have been identified; this, and other research on antlions (Myrmeleontidae), suggests that male-produced long-range pheromones are the norm for the order. Characterizations of the myriad neuropteran exocrine gland systems, including prothoracic, metathoracic, abdominal, dermal, and anal glands, are revealing unforeseen trophic relationships with biological control implications. For examples, males of Chrysopa and other lacewing genera evidently must sequester specific chemical precursors from prey or plants to produce their attractant pheromones, and larval antlion venoms are potentially important genetic leads for insecticidal peptides.

Horticulture is one of the most important agricultural subsectors in Africa, providing income, creating employment opportunities, and enhancing food and nutritional security. However, tephritid fruit flies are responsible for both direct and indirect losses, with alien invasive species often having the most severe ecological and economic impact. In the past 20 years, systematic analysis of tephritids has provided comparative information on taxonomy, synonymy, and character-state differentiation. New molecular techniques are now available for identifying species, reconstructing phylogenies, and studying population genetic structures. Research on biology, host range and shifts, thermotolerance, and demography has provided useful information for developing predictive and ecological niche models to guide management methods. In recent years, the responses of various species to attractants have been documented. Several suppression methods, including the release of coevolved parasitoid species targeting invasives, have been promoted within the context of integrated pest management, leading to improvement in the quality and quantity of fruits and vegetables produced. However, there is still the need for wide-scale availability of these technologies to smallholder growers across Africa.

Immune defense and reproduction are physiologically and energetically demanding processes and have been observed to trade off in a diversity of female insects. Increased reproductive effort results in reduced immunity, and reciprocally, infection and activation of the immune system reduce reproductive output. This trade-off can manifest at the physiological level (within an individual) and at the evolutionary level (genetic distinction among individuals in a population). The resource allocation model posits that the trade-off arises because of competition for one or more limiting resources, and we hypothesize that pleiotropic signaling mechanisms regulate allocation of that resource between reproductive and immune processes. We examine the role of juvenile hormone, 20-hydroxyecdysone, and insulin/insulin-like growth factor-like signaling in regulating both oogenesis and immune system activity, and propose a signaling network that may mechanistically regulate the trade-off. Finally, we discuss implications of the trade-off in an ecological and evolutionary context.

Insect hearing has independently evolved multiple times in the context of intraspecific communication and predator detection by transforming proprioceptive organs into ears. Research over the past decade, ranging from the biophysics of sound reception to molecular aspects of auditory transduction to the neuronal mechanisms of auditory signal processing, has greatly advanced our understanding of how insects hear. Apart from evolutionary innovations that seem unique to insect hearing, parallels between insect and vertebrate auditory systems have been uncovered, and the auditory sensory cells of insects and vertebrates turned out to be evolutionarily related. This review summarizes our current understanding of insect hearing. It also discusses recent advances in insect auditory research, which have put forward insect auditory systems for studying biological aspects that extend beyond hearing, such as cilium function, neuronal signal computation, and sensory system evolution.

The diamondback moth (DBM), Plutella xylostella (L.), costs the Chinese economy US$0.77 billion annually, and considerable research has focused on its biology, ecology, and management. Much of this research has been published locally and is inaccessible outside China. Since 1990 Brassica vegetable production has increased 20-fold and production practices have intensified, but losses continue to increase. Insecticide use is widespread and many DBM populations, particularly in southern provinces, are resistant to multiple compounds. The molecular bases of several insecticide resistance mechanisms are well understood, and genetic studies suggest that insecticide-resistant populations migrate northward in spring and that back migrations may occur in southern provinces. Fundamental studies have improved our understanding of the effects of temperature on DBM population dynamics and distributions and of interactions between DBM and its well-established parasitoid fauna. Nationally coordinated research is developing regional management strategies that integrate locally appropriate biological, physical, cultural, and insecticidal control, but sustaining their adoption will prove an enormous challenge.

Why do most animals live solitarily, while complex social life is restricted to a few cooperatively breeding vertebrates and social insects? Here, we synthesize concepts and theories in social evolution and discuss its underlying ecological causes. Social evolution can be partitioned into (a) formation of stable social groups, (b) evolution of helping, and (c) transition to a new evolutionary level. Stable social groups rarely evolve due to competition over food and/or reproduction. Food competition is overcome in social insects with central-place foraging or bonanza-type food resources, whereas competition over reproduction commonly occurs because staying individuals are rarely sterile. Hence, the evolution of helping is shaped by direct and indirect fitness options and helping is only altruism if it reduces the helper's direct fitness. The helper's capability to gain direct fitness also creates within-colony conflict. This prevents transition to a new evolutionary level.

In insects, olfaction plays a crucial role in many behavioral contexts, such as locating food, sexual partners, and oviposition sites. To successfully perform such behaviors, insects must respond to chemical stimuli at the right moment. Insects modulate their olfactory system according to their physiological state upon interaction with their environment. Here, we review the plasticity of behavioral responses to different odor types according to age, feeding state, circadian rhythm, and mating status. We also summarize what is known about the underlying neural and endocrinological mechanisms, from peripheral detection to central nervous integration, and cover neuromodulation from the molecular to the behavioral level. We describe forms of olfactory plasticity that have contributed to the evolutionary success of insects and have provided them with remarkable tools to adapt to their ever-changing environment.

Eradication is the deliberate elimination of a species from an area. Given that international quarantine measures can never be 100% effective, surveillance for newly arrived populations of nonnative species coupled with their eradication represents an important strategy for excluding potentially damaging insect species. Historically, eradication efforts have not always been successful and have sometimes been met with public opposition. But new developments in our understanding of the dynamics of low-density populations, the availability of highly effective treatment tactics, and bioeconomic analyses of eradication strategies offer new opportunities for developing more effective surveillance and eradication programs. A key component that connects these new developments is the harnessing of Allee effects, which naturally promote localized species extinction. Here we review these developments and suggest how research might enhance eradication strategies.

Ant colonies provide well-protected and resource-rich environments for a plethora of symbionts. Historically, most studies of ants and their symbionts have had a narrow taxonomic scope, often focusing on a single ant or symbiont species. Here we discuss the prospects of studying these assemblies in a community ecology context using the framework of ecological network analysis. We introduce three basic network metrics that we consider particularly relevant for improving our knowledge of ant-symbiont communities: interaction specificity, network modularity, and phylogenetic signal. We then discuss army ant symbionts as examples of large and primarily parasitic communities, and symbiotic sternorrhynchans as examples of generally smaller and primarily mutualistic communities in the context of these network analyses. We argue that this approach will provide new and complementary insights into the evolutionary and ecological dynamics between ants and their many associates, and will facilitate comparisons across different ant-symbiont assemblages as well as across different types of ecological networks.