Annual Review of Entomology - Volume 48, 2003

Vibratory signals of plant-dwelling insects, such as land bugs of the families Cydnidae and Pentatomidae, are produced mainly by stridulation and/or vibration of some body part. Signals emitted by the vibratory mechanisms have low-frequency characteristics with a relatively narrow frequency peak dominant around 100 Hz and differently expressed frequency modulation and higher harmonics. Such spectral characteristics are well tuned to the transmission properties of plants, and the low attenuation enables long-range communication on the same plant under standing wave conditions. Frequencies of stridulatory signals extend up to 10 kHz. In some groups, vibratory and stridulatory mechanisms may be used simultaneously to produce broadband signals. The subgenual organ, joint chordotonal organs, campaniform sensilla and mechanoreceptors, such as the Johnston's organ in antennae, are used to detect these vibratory signals. Species-specific songs facilitate mate location and recognition, and less species-specific signals provide information about enemies or rival mates.

Insect-plant interactions involving the cultivated tomato and its relatives in the genus Lycopersicon have been intensively studied for several decades, resulting in one of the best documented and in-depth examples of the mechanistic complexities of insect-plant interactions, which encompass both herbivores and their natural enemies. Trichome-mediated defenses are particularly significant in L. hirsutum f. glabratum and have been extensively implicated in negative tritrophic effects mediated by direct contact of parasitoids and predators with trichomes, as well as indirect effects mediated through their hosts or prey. Both constitutive and inducible defense traits of L. esculentum exert effects on selected parasitoids and predators. The effects of any particular plant defense trait on parasitoids and predators depend on the specific attributes of the plant trait and the details of the physical, biochemical, and behavioral interaction between the natural enemy, its host (prey), and the plant.

This review addresses the problems insects and ticks face to feed on blood and the solutions these invertebrates engender to overcome these obstacles, including a sophisticated salivary cocktail of potent pharmacologic compounds. Recent advances in transcriptome and proteome research allow an unprecedented insight into the complexity of these compounds, indicating that their molecular diversity as well as the diversity of their targets is still larger than previously thought.

Nervous system function is entirely dependent on the intricate and precise pattern of connections made by individual neurons. Much of the insightful research into mechanisms underlying the development of this pattern of connections has been done in insect nervous systems. Studies of developmental mechanisms have revealed critical interactions between neurons and glia, the non-neuronal cells of the nervous system. Glial cells provide trophic support for neurons, act as struts for migrating neurons and growing axons, form boundaries that restrict neuritic growth, and have reciprocal interactions with neurons that govern specification of cell fate and axonal pathfinding. The molecular mechanisms underlying these interactions are beginning to be understood. Because many of the cellular and molecular mechanisms underlying neural development appear to be common across disparate insect species, and even between insects and vertebrates, studies in developing insect nervous systems are elucidating mechanisms likely to be of broad significance.

The century-old discovery of the role of Anopheles in human malaria transmission precipitated intense study of this genus at the alpha taxonomy level, but until recently little attention was focused on the systematics of this group. The application of molecular approaches to systematic problems ranging from subgeneric relationships to relationships at and below the species level is helping to address questions such as anopheline phylogenetics and biogeography, the nature of species boundaries, and the forces that have structured genetic variation within species. Current knowledge in these areas is reviewed, with an emphasis on the Anopheles gambiae model. The recent publication of the genome of this anopheline mosquito will have a profound impact on inquiries at all taxonomic levels, supplying better tools for estimating phylogeny and population structure in the short term, and ultimately allowing the identification of genes and/or regulatory networks underlying ecological differentiation, speciation, and vectorial capacity.

Many of the most harmful parasitic diseases are transmitted by blood-feeding insect vectors. During this stage of their life cycles, selection pressures favor parasites that can manipulate their vectors to enhance transmission. Strategies may include increasing the amount of contact between vector and host, reducing vector reproductive output and consequently altering vector resource management to increase available nutrient reserves, and increasing vector longevity. Manipulation of these life-history traits may be more beneficial at some phase of the parasite's developmental process than at others. This review examines empirical, experimental, and field-based evidence to evaluate examples of changes in vector behavior and physiology that might be construed to be manipulative. Examples are mainly drawn from malaria-infected mosquitoes, Leishmania-infected sandflies, and Trypanosoma-infected tsetse flies.

Secretions of male accessory glands contain a variety of bioactive molecules. When transferred during mating, these molecules exert wide-ranging effects on female reproductive activity and they improve the male's chances of siring a significant proportion of the female's offspring. The accessory gland secretions may affect virtually all aspects of the female's reproductive activity. The secretions may render her unwilling or unable to remate for some time, facilitating sperm storage and ensuring that any eggs laid will be fertilized by that male's sperm. They may stimulate an increase in the number and rate of development of eggs and modulate ovulation and/or oviposition. Antimicrobial agents in the secretions ensure that the female reproductive tract is a hospitable environment during sperm transfer. In a few species the secretions include noxious chemicals. These are sequestered by developing eggs that are thereby protected from predators and pathogens when laid.

Birds host many lineages of symbiotic mites, but the greatest diversity is shown by the three superfamilies of astigmatan feather mites: Analgoidea, Pterolichoidea, and Freyanoidea. Members of this diphyletic grouping have colonized all parts of the avian integument from their ancestral nidicolous habitat. Whereas some clearly feed on feather pith or skin, acting as parasites, other feather mites are paraphages and consume feather oils without causing structural damage. Sexual dimorphism in feather mites is often extreme, and little is known of the function of many elaborate male structures. Abundance and location of vane-dwelling mites is affected by season, temperature, light, humidity, and host body condition. Because transmission between hosts usually depends on host body contact, it is unsurprising that feather mite phylogeny often parallels host phylogeny; however, recent cladistic analyses have also found evidence of host-jumping and “missing the boat” in several mite lineages.

Comparative analysis of the complete genome sequences of 13 baculoviruses revealed a core set of 30 genes, 20 of which have known functions. Phylogenetic analyses of these 30 genes yielded a tree with 4 major groups: the genus Granulovirus (GVs), the group I and II lepidopteran nucleopolyhedroviruses (NPVs), and the dipteran NPV, CuniNPV. These major divisions within the family Baculoviridae were also supported by phylogenies based on gene content and gene order. Gene content mapping has revealed the patterns of gene acquisitions and losses that have taken place during baculovirus evolution, and it has highlighted the fluid nature of baculovirus genomes. The identification of shared protein phylogenetic profiles provided evidence for two putative DNA repair systems and for viral proteins specific for infection of lymantrid hosts. Examination of gene order conservation revealed a core gene cluster of four genes, helicase, lef-5, ac96, and 38K(ac98), whose relative positions are conserved in all baculovirus genomes.

Genomics is the study of the structure and function of the genome: the set of genetic information encoded in the DNA of the nucleus and organelles of an organism. It is a dynamic field that combines traditional paths of inquiry with new approaches that would have been impossible without recent technological developments. Much of the recent focus has been on obtaining the sequence of entire genomes, determining the order and organization of the genes, and developing libraries that provide immediate physical access to any desired DNA fragment. This has enabled functional studies on a genome-wide level, including analysis of the genetic basis of complex traits, quantification of global patterns of gene expression, and systematic gene disruption projects. The successful contribution of genomics to problems in applied entomology requires the cooperation of the private and public sectors to build upon the knowledge derived from the Drosophila genome and effectively develop models for other insect Orders.

Ideally, integrated pest management should rely on an array of tactics. In reality, the main technologies in use are synthetic pesticides. Because of well-documented problems with reliance on synthetic pesticides, viable alternatives are sorely needed. Physical controls can be classified as passive (e.g., trenches, fences, organic mulch, particle films, inert dusts, and oils), active (e.g., mechanical, polishing, pneumatic, impact, and thermal), and miscellaneous (e.g., cold storage, heated air, flaming, hot-water immersion). Some physical methods such as oils have been used successfully for preharvest treatments for decades. Another recently developed method for preharvest situations is particle films. As we move from production to the consumer, legal constraints restrict the number of options available. Consequently, several physical control methods are used in postharvest situations. Two noteworthy examples are the entoleter, an impacting machine used to crush all insect stages in flour, and hot-water immersion of mangoes, used to kill tephritid fruit fly immatures in fruit. The future of physical control methods will be influenced by sociolegal issues and by new developments in basic and applied research.

Lacking a comprehensive fossil record, solitary representatives of the taxa, and/or a definitive phylogeny of closely related insects, comparison of the life history and social biology of basal, living groups is one of the few available options for developing inferences regarding the early eusocial evolution of ants and termites. Comparisons of a select group of basal formicid and isopteran taxa suggest that the reproductive organization of colonies and their patterns of division of labor were particularly influenced, in both groups, by nesting and feeding ecology. Opportunities for serial inheritance of the nest structure and colony population by kin may have been significant in the evolution of multiple reproductive forms and options. Disease has been a significant factor in the evolution of social organization in ants and termites, but the adaptive mechanisms of infection control differ. Evaluations of the convergent and divergent social biology of the two taxa can generate novel domains of research and testable hypotheses.

Until the 1990s, Amblyomma americanum was regarded primarily as a nuisance species, but a tick of minor importance as a vector of zoonotic pathogens affecting humans. With the recent discoveries of Ehrlichia chaffeensis, Ehrlichia ewingii, and “Borrelia lonestari,” the public health relevance of lone star ticks is no longer in question. During the next 25 years, the number of cases of human disease caused by A. americanum-associated pathogens will probably increase. Based on current trajectories and historic precedents, the increase will be primarily driven by biological and environmental factors that alter the geographic distribution and intensity of transmission of zoonotic pathogens. Sociologic and demographic changes that influence the likelihood of highly susceptible humans coming into contact with infected lone star ticks, in addition to advances in diagnostic capabilities and national surveillance efforts, will also contribute to the anticipated increase in the number of recognized cases of disease.

Neonicotinoids, the most important new class of synthetic insecticides of the past three decades, are used to control sucking insects both on plants and on companion animals. Imidacloprid (the principal example), nitenpyram, acetamiprid, thiacloprid, thiamethoxam, and others act as agonists at the insect nicotinic acetylcholine receptor (nAChR). The botanical insecticide nicotine acts at the same target without the neonicotinoid level of effectiveness or safety. Fundamental differences between the nAChRs of insects and mammals confer remarkable selectivity for the neonicotinoids. Whereas ionized nicotine binds at an anionic subsite in the mammalian nAChR, the negatively tipped (“magic” nitro or cyano) neonicotinoids interact with a proposed unique subsite consisting of cationic amino acid residue(s) in the insect nAChR. Knowledge reviewed here of the functional architecture and molecular aspects of the insect and mammalian nAChRs and their neonicotinoid-binding site lays the foundation for continued development and use of this new class of safe and effective insecticides.

Controversy exists over ecological risks in classical biological control. We reviewed 10 projects with quantitative data on nontarget effects. Ten patterns emerged: (a) Relatives of the pest are most likely to be attacked; (b) host-specificity testing defines physiological host range, but not ecological range; (c) prediction of ecological consequences requires population data; (d) level of impact varied, often in relation to environmental conditions; (e) information on magnitude of nontarget impact is sparse; (f) attack on rare native species can accelerate their decline; (g) nontarget effects can be indirect; (h) agents disperse from agroecosystems; (i) whole assemblages of species can be perturbed; and (j) no evidence on adaptation is available in these cases. The review leads to six recommendations: Avoid using generalists or adventive species; expand host-specificity testing; incorporate more ecological information; consider ecological risk in target selection; prioritize agents; and pursue genetic data on adaptation. We conclude that retrospective analyses suggest clear ways to further increase future safety of biocontrol.

There are three major classes of insect genetic systems: those with diploid males (diplodiploidy), those with effectively haploid males (haplodiploidy), and those without males (thelytoky). Mixed systems, involving cyclic or facultative switching between thelytoky and either of the other systems, also occur. I present a classification of the genetic systems of insects and estimate the number of evolutionary transitions between them that have occurred. Obligate thelytoky has arisen from each of the other systems, and there is evidence that over 900 such origins have occurred. The number of origins of facultative thelytoky and the number of reversions from obligate thelytoky to facultative and cyclic thelytoky are difficult to estimate. The other transitions are few in number: five origins of cyclic thelytoky, eight origins of obligate haplodiploidy (including paternal genome elimination), the strange case of Micromalthus, and the two reversions from haplodiploidy to diplodiploidy in scale insects. Available evidence tends to support W.D. Hamilton's hypothesis that maternally transmitted endosymbionts have been involved in the origins of haplodiploidy. Bizarre systems of extrazygotic inheritance in Sternorrhyncha are not easily accommodated into any existing classification of genetic systems.

Recent application of biochemical and molecular techniques to study the genesis of scolytid aggregation pheromones has revealed that bark beetles are primarily responsible for the endogenous synthesis of widely occurring pheromone components such as ipsenol, ipsdienol, and frontalin. Because many of the chemical signals are isoprenoids, the roles of the mevalonate biosynthetic pathway and the enzyme HMG-CoA reductase (HMG-R) have been investigated. This has led to the identification of endothelial cells in the anterior midgut as the site of synthesis and to the concept that de novo pheromone biosynthesis is regulated in part by the positive effect of juvenile hormone III (JHIII) on gene expression for HMG-R. Both the pronounced regulation by JHIII and the expression pattern of eukaryotic HMG-R argue against synthesis of these pheromones by prokaryotes. As the mevalonate pathway and its regulation have been studied in few other insects, broader issues addressed through the study of scolytid pheromone biosynthesis include major step versus coordinate regulation of the pathway and a genomics approach to elucidating the entire pathway and the mode of action of JHIII.

Gustatory receptors associated with feeding in phytophagous insects are broadly categorized as phagostimulatory or deterrent. No phytophagous insect is known that tastes all its essential nutrients, and the ability to discriminate between nutrients is limited. The insects acquire a nutritional balance largely “adventitiously” because leaves have an appropriate chemical composition. Sugars are the most important phagostimulants. Plant secondary compounds are most often deterrent but stimulate phagostimulatory cells if they serve as host-indicating sign stimuli, or if they are sequestered for defense or used as pheromone precursors. The stimulating effects of chemicals are greatly affected by other chemicals in mixtures like those to which the sensilla are normally exposed. Host plant selection depends on the balance of phagostimulatory and deterrent inputs with, in some oligophagous and monophagous species, a dominating role of a host-related chemical. Evolution of phytophagy has probably involved a change in emphasis in the gustatory system, not fundamentally new developments. The precise role of the gustatory systems remains unclear. In grasshoppers, it probably governs food selection and the amounts eaten, but in caterpillars there is some evidence that central feedbacks are also involved in regulating the amount eaten.