Annual Review of Entomology - Volume 46, 2001

Insects of the order Hymenoptera are biologically and economically important members of natural and agro ecosystems and exhibit diverse biologies, mating systems, and sex pheromones. We review what is known of their sex pheromone chemistry and function, paying particular emphasis to the Hymenoptera Aculeata (primarily ants, bees, and sphecid and vespid wasps), and provide a framework for the functional classification of their sex pheromones. Sex pheromones often comprise multicomponent blends derived from numerous exocrine tissues, including the cuticle. However, very few sex pheromones have been definitively characterized using bioassays, in part because of the behavioral sophistication of many Aculeata. The relative importance of species isolation versus sexual selection in shaping sex pheromone evolution is still unclear. Many species appear to discriminate among mates at the level of individual or kin/colony, and they use antiaphrodisiacs. Some orchids use hymenopteran sex pheromones to dupe males into performing pseudocopulation, with extreme species specificity.

Biodemography is an emerging subdiscipline of classical demography that brings life table techniques, mortality models, experimental systems, and comparative methods to bear on questions concerned with the fundamental determinants of mortality, longevity, aging, and life span. It is important to entomology because it provides a secure and comprehensive actuarial foundation for life table and mortality analysis, it suggests new possibilities for the use of model insect systems in the study of aging and mortality dynamics, and it integrates an interdisciplinary perspective on demographic concepts and actuarial techniques into the entomological literature. This paper describes the major life table formulae and mortality models used to analyze the actuarial properties of insects; summarizes the literature on adult insect life span, including a discussion of basic concepts; identifies the major correlates of extended longevity; and suggests new ideas for using demographic concepts in both basic and applied entomology.

St. Louis encephalitis virus was first identified as the cause of human disease in North America after a large urban epidemic in St. Louis, Missouri, during the summer of 1933. Since then, numerous outbreaks of St. Louis encephalitis have occurred throughout the continent. In south Florida, a 1990 epidemic lasted from August 1990 through January 1991 and resulted in 226 clinical cases and 11 deaths in 28 counties. This epidemic severely disrupted normal activities throughout the southern half of the state for 5 months and adversely impacted tourism in the affected region. The accurate forecasting of mosquito-borne arboviral epidemics will help minimize their impact on urban and rural population centers. Epidemic predictability would help focus control efforts and public education about epidemic risks, transmision patterns, and elements of personal protection that reduce the probability of arboviral infection. Research associated with arboviral outbreaks has provided an understanding of the strengths and weaknesses associated with epidemic prediction. The purpose of this paper is to review lessons from past arboviral epidemics and determine how these observations might aid our ability to predict and respond to future outbreaks.

Exclusive male care of offspring is the rarest form of postzygotic parental care among animals and has arisen independently in only 13 arthropod taxa. To distinguish the effects of sexual selection from those of natural selection on the evolution of arthropod paternal care, predictions concerning several life-history and behavioral traits resulting from both forms of selection are made and tested across all known taxa with exclusive paternal care. Comparisons suggest parallels between prezygotic nuptial gifts and exclusive postzygotic male care and support the hypothesis that, in arthropods, male behaviors that enhance female reproductive success either directly, by releasing females from the fecundity constraints of maternal care (enhanced fecundity hypothesis), or indirectly, by identifying mates with superior genes (handicap principle), are traits on which sexual selection has acted. Under such conditions, males that are willing to guard young become preferred mates for gravid females and enjoy greater promiscuity than males that are unable or unwilling to guard. Females use nest construction or the act of guarding another female's eggs as honest signals of paternal intent and quality.

Mate-seeking and sperm-transfer in the ixodid hard ticks, which include important vectors of zoonotic pathogens, generally reflect their peculiarly prolonged pattern of feeding. The metastriate ticks, including Dermacentor, Amblyomma, and Rhipicephalus, invariably attain sexual maturity and mate solely on their hosts. The more primitive prostriate Ixodes ticks, however, may copulate both in the absence of hosts and while the female engorges. These expanded opportunities for insemination complicate the mating systems of the Ixodes ricinus complex of species. In these ticks, autogenous spermatogenesis must precede host contact, whereas anautogenous oogenesis requires that the females store sperm. All hard tick males undergo a courting ritual before they can deposit their spermatophores within the female's genital tract. These diverse and prolonged patterns of sexual interaction provide opportunities for interactions between populations and individuals that may be relevant to the role of ticks as vectors of zoonotic pathogens.

The genetic background of individual mosquito species and populations within those species influences the transmission of mosquito-borne pathogens to humans. Technical advances in contemporary genomics are contributing significantly to the detailed genetic analysis of this mosquito-pathogen interaction as well as all other aspects of mosquito biology, ecology, and evolution. A variety of DNA-based marker types are being used to develop genetic maps for a number of mosquito species. Complex phenotypic traits such as vector competence are being dissected into their discrete genetic components, with the intention of eventually using this information to develop new methods to prevent disease transmission. Both genetic- and physical-mapping techniques are being used to define and compare genome architecture among and within mosquito species. The integration of genetic- and physical-map information is providing a sound framework for map-based positional cloning of target genes of interest. This review focuses on advances in genome-based analysis and their specific applications to mosquitoes.

Acid-base status influences many aspects of insect biology, including insect distributions in aquatic systems, insect-plant and insect-pathogen interactions, membrane transport phenomena, and the mode of action of pesticides. Acid-base status in the hemolymph and gut lumen of insects is generally well regulated but varies somewhat within individuals owing to effects of temperature, activity, discontinuous ventilation, and diet. The pH of the midgut lumen varies with the phylogeny and feeding ecology. Insect fluids have buffer values similar to those of vertebrates. The respiratory system participates in acid-base homeostasis primarily by regulating the internal carbon dioxide (partial) pressure via changes in spiracular opening and convective ventilation. The epithelia of the renal system and gut participate in hemolymph acid-base regulation by varying acid-base transport in response to organismal acid-base status. Evidence to date suggests that the dominant mechanisms for control of renal acid-base excretion involve hormonal regulation of H⁺-V-ATPase activity.

In almost all species of parasitic wasps in the Coccophaginae, a subfamily of Aphelinidae, males have host relationships different from females. In these “heteronomous” species, females are generally endoparasitoids of sternorrhynchous Hemiptera, such as scale insects, mealybugs, and whiteflies. In contrast, males may be hyperparasitoids, developing in or on conspecific females or other primary parasitoids. In other species, females are endoparasitoids of whiteflies, and males are primary endoparasitoids of eggs of Lepidoptera. Males and females may both be primary parasitoids on the same species of scale insect hosts, but females develop as endoparasitoids, whereas males are ectoparasitoids. Here we review these life histories, focusing on examples of sexually dimorphic host relationships, development, and morphology. Coccophagine species may be sexual or parthenogenetic; we discuss reproductive modes and the interaction of sex ratio distorters with sex-specific host relationships. Sex allocation in the species in which males are hyperparasitoids involves choices of not what sex egg to lay, but whether to accept or reject a host of a given type; study in this area is reviewed as well as research in kin discrimination and ovicide. Last, we present the current understanding of phylogenetic relationships within this lineage and discuss hypotheses for the evolutionary origin of heteronomy in the Aphelinidae.

The role that entomology has played in the historical (1800s–1970s) development of ecological theories that match species traits with environmental constraints is reviewed along three lineages originating from the ideas of a minister (Malthus TR. 1798. An Essay on the Principle of Population. London: Johnson) and a chemist (Liebig J. 1840. Die Organische Chemie in ihrer Anwendung auf Agricultur und Physiologie. Braunschweig: Vieweg). Major developments in lineage 1 focus on habitat as a filter for species traits, succession, nonequilibrium and equilibrium conditions, and generalizations about the correlation of traits to environmental constraints. In lineage 2, we trace the evolution of the niche concept and focus on ecophysiological traits, biotic interactions, and environmental conditions. Finally, we describe the conceptual route from early demographic studies of human and animal populations to the r-K concept in lineage 3. In the 1970s, the entomologist Southwood merged these three lineages into the “habitat templet concept” (Southwood TRE. 1977. J. Anim. Ecol. 46:337–65), which has stimulated much subsequent research in entomology and general ecology. We conclude that insects have been a far more important resource for the development of ecological theory than previously acknowledged.

The past 5 years have witnessed the emergence of techniques that permit the stable genetic transformation of a number of non-drosophilid insect species. These transposable-element-based strategies, together with virus-based techniques that allow the expression of genes to be quickly examined in insects, provide insect scientists with a first generation of genetic tools that can begin to be harnessed to further increase our understanding of gene function and regulation in insects. We review and compare the characteristics of these gene transfer systems and conclude that, although significant progress has been made, these systems still do not meet the requirements of robust genetic tools. We also review risk assessment issues arising from the generation and probable release of genetically engineered insects.

Reproductive-skew theory can be broadly divided into transactional models, in which reproduction is shared among group members in return for some fitness benefit, and tug-of-war models, in which reproductive sharing arises solely from an inability of each group member to fully control the others. For small-colony social insects in which complete reproductive control by a single individual is plausible, transactional-concession models account, better than any other existing model, for observed relationships between each of the dependent variables of skew, changes in reproductive partitioning over time, group size, and within-group aggression, and each of the predictor variables of genetic relatedness, ecological constraints on solitary breeding, and benefits of group living. An extension of transactional-concession models via the “workers-as-a-collective-dominant” model potentially offers new insights into some of the most striking reproductive patterns in large-colony eusocial Hymenopteran species, from the loss of worker capacity to produce female offspring to patterns of skew and aggression in polygynous societies.

Grape phylloxera, Daktulosphaira vitifoliae (Homoptera: Phylloxeridae), is a worldwide pest of grapevines. Its life cycle has sexual and asexual portions with forms that feed from leaf and root galls. Not all forms occur throughout the insect's range. Root forms predominate on Vitis vinifera cultivars; leaf forms predominate on other Vitis species characteristic of the American native range. Other conditions influence expression of the life cycle. Hosts and conditions similarly affect life table performance. Damage to grapevines is by secondary soilborne pathogens attacking the feeding site and by physiological interaction of the insect with the grapevine, though the latter has not been well studied. Resistant rootstocks derived from native American Vitis are the primary control tool. The insect varies genetically and relative to performance on hosts. Use of insecticides is limited in effect, and other control methods are not proven. More research on the biology, ecology, and management of phylloxera is needed.

Division of labor is one of the most basic and widely studied aspects of colony behavior in social insects. Studies of division of labor are concerned with the integration of individual worker behavior into colony level task organization and with the question of how regulation of division of labor may contribute to colony efficiency.

Here we describe and critique the current models concerned with the proximate causes of division of labor in social insects. The models have identified various proximate mechanisms to explain division of labor, based on both internal and external factors. On the basis of these factors, we suggest a classification of the models. We first describe the different types of models and then review the empirical evidence supporting them.

The models to date may be considered preliminary and exploratory; they have advanced our understanding by suggesting possible mechanisms for division of labor and by revealing how individual and colony-level behavior may be related. They suggest specific hypotheses that can be tested by experiment and so may lead to the development of more powerful and integrative explanatory models.

Modern population genetics underwent a major paradigm shift during the last decade of the 20th century with the discovery that thousands of genes of known function and position in a genome can be analyzed simultaneously in a single individual. The impact of this technology on insect population genetics is potentially profound. Sampling distributions of genetic statistics can now be derived from many individual loci or among many segregating sites within a gene. Inferences regarding random mating, gene flow, effective population sizes, disequilibrium, and relatedness among populations can now be based on patterns of variation at many loci. More importantly, genome-wide sampling enables population geneticists to distinguish effects that act on the whole genome from those that act on individual loci or nucleotides. We introduce the term “population genomics” to describe the process of simultaneous sampling of numerous variable loci within a genome and the inference of locus-specific effects from the sample distributions. The four critical assumptions implicit in the population genomics approach are explained in detail. Studies adopting this paradigm are reviewed, and the steps necessary to complete a population genomics study are outlined.

We review the physiological, molecular, and neural mechanisms of insect color vision. Phylogenetic and molecular analyses reveal that the basic bauplan, UV-blue-green-trichromacy, appears to date back to the Devonian ancestor of all pterygote insects. There are variations on this theme, however. These concern the number of color receptor types, their differential expression across the retina, and their fine tuning along the wavelength scale. In a few cases (but not in many others), these differences can be linked to visual ecology. Other insects have virtually identical sets of color receptors despite strong differences in lifestyle. Instead of the adaptionism that has dominated visual ecology in the past, we propose that chance evolutionary processes, history, and constraints should be considered. In addition to phylogenetic analyses designed to explore these factors, we suggest quantifying variance between individuals and populations and using fitness measurements to test the adaptive value of traits identified in insect color vision systems.

Tracking the movement of insects in their natural habitat is essential for understanding their basic biology, demography, and ethology. A wide variety of markers have been used to assess insect population dynamics, dispersal, territoriality, feeding behavior, trophic-level interactions, and other ecological interactions. The ideal marker should persist without inhibiting the insect's “normal” biology. Furthermore, the marker should be environmentally safe, cost–effective, and easy to use. In this article, we review the current state of knowledge regarding insect marking, document the advantages and limitations of each marking technique, and discuss advances made in marking insects over the past decade.

Insects, including Drosophila, readily respond to toxins such as phytotoxins, metal ions, and insecticides in their environment by evolving resistance. Although Drosophila are seldom targets for insecticides, nevertheless populations worldwide have evolved resistance to a variety of insecticides, and these resistance alleles persist in high frequency. In many cases, Drosophila use the same genetic and biochemical mechanisms that underlie resistance in pest insects, including single-site changes in target molecules resulting from point mutations and upregulation of degradative enzymes, particularly cytochrome P450 enzymes and glutathione S-transferases. However, several types of resistance found in pest insects, such as gene amplification and knock-down resistance, have not been reported in Drosophila field populations. Excellent Drosophila-plant models are being studied to understand the adaptation to phytotoxins; P450 enzymes are clearly involved in phytotoxin resistance in one of these models. The genetic advantages of D. melanogaster, including availability of the sequenced genome, should allow further study of these genes and identification of new ones, particularly regulatory genes, responsible for resistance.

The chemical strategies by which parasites manage to break into the social fortresses of ants offer a fascinating theme in chemical ecology. Semiochemicals used for interindividual nestmate recognition are also involved in the mechanisms of tolerance and association between the species, and social parasites exploit these mechanisms. The obligate parasites are odorless (“chemical insignificance”) at the time of usurpation, like all other callow ants, and this “invisibility” enables their entry into the host colony. By chemical mimicry (sensu lato), they later integrate the gestalt odor of this colony (“chemical integration”). We hypothesize that host and parasite are likely to be related chemically, thereby facilitating the necessary mimicry to permit bypassing the colony odor barrier. We also review the plethora of chemical weapons used by social parasites (propaganda, appeasement, and/or repellent substances), particularly during the usurpation period, when the young mated parasite queen synthesizes these chemicals before usurpation and ceases such biosynthesis afterwards. We discuss evolutionary trends that may have led to social parasitism, focusing on the question of whether slave-making ants and their host species are expected to engage in a coevolutionary arms race.